10
Sleep Disturbances in Children With Attention-Deficit/Hyperactivity Disorder PENNY CORKUM, M.A., ROSEMARYTANNOCK, PH.D., AND HARVEY MOLDOFSKY, M.D. ABSTRACT ObJective: To evaluate the relationship between sleep disturbances and attention-def icitlhyperact ivity disorder (ADHD). Method: Empirical research published since 1970 on sleep disturbances in children with ADHD was systemat ically reviewed. A "box-score" approach was used to examine consistency of findings across the studies, which used different outcome measures. Results: Although subjective accounts of sleep disturbances in ADHD were prevalent, objective verification of these disturbances was less robust. The only consistent objective findings were that children with ADHD displayed more movements during sleep but did not differ from normal controls in total sleep time. An additional finding was that stimulant medication led to changes in the children's sleep (e.g., prolonged sleep latency, increased length of onset to first rapid eye movement cycle), but these changes were believed to be nonpathological. Conclusions: The exact nature of the sleep problems in children with ADHD remains to be determined. Many of the relevant issues have not been adequately addressed . Factors such as poorly defined diagnostic groups, small sample sizes, few studies , and methodological and procedural limitations make it difficult to determine the relationship between ADHD and sleep problems. J. Am. Acad. Child Ado/esc. Psychiatry, 1998, 37(6) :637-646. Key Words: attention-deficitlhyperactivity disorder, sleep, stimulant medication. Attention-deficit/hyperactivity disorder (ADHD) is the most common problem presented to children's mental health services. The disorder affects approximately 5% of school-age children (American Psychiatric Associa- tion, 1994). ADHD is characterized as a heterogeneous combination of several disruptive behaviors, academic underachievement, and poor social relations (e.g., Barkley, 1990). The core symptoms of this disorder include varying degrees of inattention, impulsiveness, and restlessness. Because these symptoms have been long known to be characteristics of sleep deprivation Acceptedjanuary 15. /998. Ms. Corkum is a doctoral candidate at the Ontario Institute fOr Studies in Education. University of Toronto. Dr. Tannock isa senior researchscientist in thr Department of Psychiatry Research, Hospital fOr Sick Children, and Associate Professor of Psychiatry. Un iversity of Toronto. D r. Moldo fiky is Director. University of Toronto Centre fOr Slu p and Chronobiology. Toronto Hospital. Div ision. and Pro ftssor of Psychiatry and Medicine, Unioersity of Toronto. This project was fimdrd by the Ont ario M ental Health Foundati on. The autho rs thank Pearl Rimer and Hmk v"n Vo om fOr their editorial comments and Rusull SchacharfOr his supp ort ofthis project. Reprint rr1ums to Ms. Corkum. Department ofPsychiatry Rrsearch,Hospital fOr Sick Ch ildrm. 555 University A vmur. Toronto. Onta rio. Canada M 5G I X8; e-mai l: pcorkum @oiu .utoronto.ca 0890-8567/98/3706-0637/S03.00/0©1998 by the American Academy of Child and Adolescent Psychiatry. J. AM . ACAD . CHILD ADOLE SC. PSYC H IAT RY. 37 :6 . J UNE 1')9 8 (Kleitrnan, 1965), the role of sleep-wakefulness in ADHD merits close scrutiny. Indeed, Weinberg and Brumback (1990) speculated about a disorder similar to ADHD, named "primary disorder of vigilance." Many of the characteristics of primary disorder of vigilance overlap with those of ADHD; however, there is a sub- stant ial focus on sleepiness in children with primary dis- order of vigilance. Problems with sleep have been associated with ADHD and were previously included as one of the DSM-JII diagnostic criteria for attention deficit dis- order, although it has not been included in the last two versions of the DSM (American Psychiatric Association, 1980, 1987, 1994). Sleep problems are also currently included on a number of child rating scales used as part of the diagnostic procedures for ADHD (e.g., Conners Parent Rating Scale) (Goyette et al., 1978). The ration- ale for including these items appears to be based on clinical observations which identified an association between ADHD and sleep disturbances, rather than a theory which implicates sleep disturbances in ADHD . Sleep is known to be affected by environmental factors, genetic factors, medical factors, and biological influences. Therefore , the study of sleep in children with 637

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Page 1: Sleep Disturbances in Children With Attention‐Deficit/Hyperactivity Disorder

Sleep Disturbances in Children WithAttention-Deficit/Hyperactivity Disorder

PENNY CORKUM, M.A., ROSEMARYTANNOCK, PH.D., AND HARVEY MOLDOFSKY, M.D.

ABSTRACT

ObJective: To evaluate the relationship between sleep disturbances and attention-def icitlhyperact ivity disorder (ADHD).

Method: Empirical research published since 1970 on sleep disturbances in children with ADHD was systemat ically

reviewed. A "box-score" approach was used to examine consistency of findings across the studies, which used different

outcome measures. Results: Although subjective accounts of sleep disturbances in ADHD were prevalent, objective

verification of these disturbances was less robust. The only consistent objective findings were that children with ADHD

displayed more movements during sleep but did not differ from normal controls in total sleep time. An additional finding

was that stimulant medication led to changes in the children's sleep (e.g., prolonged sleep latency, increased length of

onset to first rapid eye movement cycle), but these changes were believed to be nonpathological. Conclusions: The

exact nature of the sleep problems in children with ADHD remains to be determined. Many of the relevant issues have

not been adequately addressed . Factors such as poorly defined diagnostic groups, small sample sizes, few studies, and

methodological and procedural limitations make it difficult to determine the relationsh ip between ADHD and sleep

problems. J. Am. Acad. Child Ado/esc. Psychiatry, 1998, 37(6) :637-646. Key Words: attention-deficitlhyperactivity

disorder, sleep, stimulant medication.

Attention-deficit/hyperactivity disorder (ADHD) is themost common problem presented to children's mentalhealth services. The disorder affects approximately 5%of school-age children (American Psychiatric Associa­tion, 1994). ADHD is characterized as a heterogeneouscombination of several disruptive behaviors, academicunderachievement, and poor social relations (e.g.,Barkley, 1990). The core symptoms of this disorderinclude varying degrees of inattention, impulsiveness,and restlessness. Because these symptoms have beenlong known to be characteristics of sleep deprivation

Acceptedjanuary 15. /998.Ms. Corkum is a doctoral candidate at the Ontario Institute fOr Studies in

Education. University of Toronto. Dr. Tannock is a senior research scientist in thr

Department ofPsychiatry Research, Hospital fOr Sick Children, and AssociateProfessor of Psychiatry. Un iversity of Toronto. D r. Moldofiky is Director.University of Toronto Centre fOr Slu p and Chronobiology. Toronto Hospital.

~sttrn Div ision. and Proftssor ofPsychiatry and Medicine, Unioersity of Toronto.Th is project was fimdrd by the Ontario M ental Health Foundation. The

autho rs thank Pearl Rimer and Hmk v" n Voom fOr their editorial commentsand Rusull SchacharfOr his support ofthis project.

Reprint rr1ums to Ms. Corkum. Department ofPsychiatry Rrsearch, Hospital

fOr Sick Childrm. 555 University Avmur. Toronto. Ontario. Canada M 5GIX8; e-mai l: pcorkum @oiu .utoronto.ca

0890-8567/98/3706-0637/S03.00/0©19 98 by the American Academyof Child and Adolescent Psychiatry.

J. AM . ACAD . C H I LD A D O LE SC. PSYC H IAT RY. 37 :6 . J UNE 1')9 8

(Kleitrnan, 1965), the role of sleep-wakefulness inADHD merits close scrutiny. Indeed, Weinberg andBrumback (1990) speculated about a disorder similar toADHD, named "primary disorder of vigilance." Manyof the characteristics of primary disorder of vigilanceoverlap with those of ADHD; however, there is a sub­stant ial focus on sleepiness in children with primary dis­order of vigilance.

Problems with sleep have been associated withADHD and were previously included as one of theDSM-JII diagnostic criteria for attention deficit dis­order, although it has not been included in the last twoversions of the DSM (American Psychiatric Association,1980, 1987, 1994). Sleep problems are also currentlyincluded on a number of child rating scales used as partof the diagnostic procedures for ADHD (e.g., ConnersParent Rating Scale) (Goyette et al., 1978). The ration­ale for including these items appears to be based onclinical observations which identified an associationbetween ADHD and sleep disturbances, rather than atheory which implicates sleep disturbances in ADHD.

Sleep is known to be affected by environmentalfactors, genetic factors, medical factors, and biologicalinfluences. Therefore , the study of sleep in children with

637

Page 2: Sleep Disturbances in Children With Attention‐Deficit/Hyperactivity Disorder

CORKUM ET AI..

ADHD allows for the opportunity to begin to evaluatethe relative importance of biological and psychosocialfactors. to evaluate variou s theories of ADHD. and toexplore the possibility of various underlying etiologie sof the subtypes and com orbid conditions of ADHD.Although there exist many clinical observat ions andtheoretical speculations regarding th e relationshipbetween ADHD and sleep disturbances. there is littleempirical research on this topic . and the prevalence andsignificance of sleep di sturbances in children withADHD remains unknown.

To help understand the relationship between ADHDand sleep. we systematically reviewed rhe literature since1970. We conducted a Medline search using specificsearch criteria and then cross-referenced these art icles.We limited our search to manuscripts published in theEnglish language in peer-reviewed journals. Sixteenstudies were found wh ich directly addressed sleep inchildren with ADHD in compa rison with normallydeveloping ch ild ren (Busby et al., 1981 ; Busby andPivik, 1985; Feinberg et al., 1974; Greenhill et al., 1983;Haig et al. , 1974 ; Kaplan et al., 198 7; Khan andRechrschaffen , 1978; Nah as and Krynicki, 1977; Palmet al., 1992; Poitras et al., 1981; Porrin o et al., 1983;Ramos Platen et al., 1990 ; Small et al., 1971; Stahlet al., 1979 ; Tirosh et al., 1993; Trommer et al., 1988) .Among these 16 stud ies. 8 studies also examined theimpact of stimulant medication on sleep in child renwith ADHD. Also. a number of other relevant studieswere reviewed: (1) studies that examined the impact ofstimulant medication on sleep in children with ADHDbut did not include baseline comparisons of ADHDand normal control children (Ch atoor er al., 1983; Kenter al., 1995; Stein et al., 1996); (2) studies in which dif­ferent methodologies were used (e.g., case study designs)(Bergman. 1976; Dahl er al., 1991) ; (3) studies in whichthe focus was on ch ildren with sleep disorders ratherthan children with ADHD (Ali et al., 1996 ; Hickeyet al. , 1992 ; Picchierri and Walters. 1994 ); and (4)studies that examined pharmacological interventions forstimulant-induced sleep problems (Brown and Gammon.1992; Prince et al., 1996) . A "box-score" approach waschosen to examine the 16 studies. with the remainingstudies used to provide additional information. A "box­score" approach allows for comparison across studiesthat differ on a number of methodological issues (e.g.•definition of ADHD, inclu sion and exclusion criterion ,type of recording) . This method was considered more

638

appropriate than meta-analysis because many of thestudies did not use the same outcome measures (whichis a necessary prerequisite for conducting a meta­an alysis). It is believed that consistency in findingsacross studies may indicate better reliability than can beinferred from the original individual study. Also, incon­sistencies in findings can indicate where statisticallysignificant findings in a small sample may be a result ofa chance occurrence.

The pr imar y goal of this review was to explore thefrequency. type . and significance of sleep problems inchildren with ADHD. Prior to reviewing this literature,we begin with a brief explanation of sleep disorders andthe me asurement of sleep in order to highlightpertinent issues. For a more detailed overview, seeAnders and Eiben (1997), Ferber and Kryger (1995) , orStores (1996).

SLEEP DISORDERS AND MEASUREMENT

TECHNIQUES

Sleep research can be divided into two general areasbased on th e method used for assessing sleepproblems-subjective and objective measures (Wiggsand Stores, 1995 ). Subjective measures (e.g., sleepd iaries, quest ionnaires, interviews) focus on theobservable aspects of sleep. such as duration of sleep.time to fall asleep, number of night wakings, numberand duration of naps. etc. These measures tend to beretrospect ive in nature , with the except ion of sleepdiaries, which are a daily log of sleep variable s recordedby the patient and/or observer.

Objective measures of sleep (e.g., polysomnographs,actigraphy, video ) typ ically capture information that isnot observable by the human eye and are recorded inreal time. Polysomnographs, which are considered the"gold standard" of sleep research , ent ail recording mul­tiple physiological measures during sleep in a laboratorysett ing (Anch er al., 1988) . Polysomnographs allow theresearcher to examine the stages of EEG sleep andarchitecture (e.g.• timing and duration of non-rapid eyemovement [NREM] stages and rapid eye movement[REM] sleep). Actigraphy uses small wrist watch-likecom puterized devices to quantify body mo vem entsduring sleep. Actigraphy distinguishes between sleepand wake stages. as well as the total duration of sleep.number of arousals, length of sleep onset, etc. Videorecordings have also been used to objectively observe

J . AM . ACAD . C H Il.D ADOI.ESC. PSYCHIATRY, .H: 6 . JUNE 19 9 8

Page 3: Sleep Disturbances in Children With Attention‐Deficit/Hyperactivity Disorder

sleep behaviors. However, neither actigraphy nor videorecordings allow the researcher to examine EEG sleepstages and architecture.

METHODOLOGICAL ISSUES IN SLEEP

RESEARCH WITH ADHD

The majority of the studies reviewed suffer from smallsample sizes (Table 1). The two subjective studies(Kaplan et al., 1987; Trommer et al., 1988) consisted of113 children with ADHD. 65 of whom were pre­schoolers. This is obviously not equivalent to epidemio­logical data. Moreover. the number of children includedin the 14 objective studies was small (91 ADHD subjectsin total) .

Diagnostic criteria and procedures varied over thestudies reviewed and may account for many of theinconsistent findings. Diagnostic procedures rangedfrom "previously diagnosed" to using parent and teacherinterviews and rating scales. Six of the 14 studies reliedon previous diagnosis and/or did not state theirdiagnostic criteria. Some studies selected for childrenwith ADHD who exhibited hyperactivity. whereasother studies did not make this distinction. Two otherstudies were not based on children with a diagnosis ofADHD. but used different diagnostic criteria (Nahasand Krynicki, 1977; Palm et al., 1992). More than halfof the studies did not report exclusionary criteria, andmost studies did not screen for comorbid disorders(Table I) .

Many children included in these studies were notmedication-naive. In fact, only one study stipulated thisas an inclusion criterion (Tirosh et al., 1993) . Somestudies ensured medication-free periods prior tosubjects' participation in the study (Greenhill et al. ,1983; Nahas and Krynicki , 1977; Poitras et al., 1981;Ramos Platon er al., 1990). The type of stimulantmedication varied (methylphenidate. dextroampheta­mine. or pemoline), as well as the dose and schedule ofmedication administration.

Inadequate control procedures were also character­istic of the majority of these studies. Often the com­parison group was not equally matched for gender. Forexample. whereas the majority of the ADHD sample(90%) were male. the comparison group included alarger proportion of females. The wide range of agesmay also account for inconsistencies in findings , withthe ages of the children varying across the studies from6 to 12 years. Even though sexual developmental stage

J . AM. ACAD . CHIl. D ADOL ESC. PSY C HIATRY, .37:6 , J UNE 1998

SLEEP DISTURBAN C ES IN ADHD

has been previously documented to be related to sleepvariables , only two studies ascertained this information(Palm et al. , 1992; Ramos Platen et al. , 1990). Twostudies used normative data for a comparison groupthat were collected in different laboratories. at differenttimes. using different procedures (Nahas and Krynicki,1977; Ramos Platon et al., 1990) . Inadequate controlprocedures are particularly problematic in this type ofresearch because of the changes in EEG sleep over theage span and differences between gender and pre­pubertal and pubertal children (Guilleminaulr, 1987).

The type, number and manner of assessing sleepparameters varied across studies. Variation in themeasurement of these parameters makes it difficult toassess the actual differences in ADHD children com­pared with normal controls across the studies reviewed.Also. there have been reservations about the use ofstandard polysomnographic scoring techniques whenapplied to children. Coble et al. (1984) comparedchildren with conduct disorder and normal controlsand found no differences on standard sleep measure­ments, but they found differences with the applicationof computerized automated measurement techniques(i.e .• delta wave counts were higher in subjects withconduct disorder).

The days of the week on which the recordings werecollected were not documented in most studies. Porrinoet al. (1983) found that children with ADHD had moremovements during sleep on weekdays than on week­ends. However, various parameters were not controlled(e.g.• differences in bedtimes on weekdays and week­ends). None of the research studies examined psycho­social variables that may account for differences in sleep(e.g.• bedtime routines). The influence of culture andfamily on sleep patterns was also not assessed in anystudy. For example, Sheldon (1996) documented thatcultural differences in child-rearing strongly influencesleep patterns and practices (e.g.• transitional objects,thumb-sucking. and breast-feeding).

The use of polysomnographic techniques withchildren raises a number of procedural issues. The sleeplaboratory is an unfamiliar environment and could bethreatening to most children (e.g.• sleeping away fromhome. wires being attached to the child's scalp). Theymay not be set up in a manner that is comforting to achild (e.g. , adjoining parent room , decorated forchildren) . In fact, Palm et al. (1992) found that childrenwith attention disorders tolerated procedures for sleep

639

Page 4: Sleep Disturbances in Children With Attention‐Deficit/Hyperactivity Disorder

Subject Characteristics

TABLE 1Subject Selection Procedures for Objective Sleep Studies~o

;l>­

:::;l>­n;l>­

oo:r:r­o;l>­oCr­t'Menn~

en-<o:r:;l>­-i

":<"""c-.

cZm

Auth ors ADHO NC Type of Record ing

Tirosh et al.• 1993No. of males and females 3 F. 8 M 20 • Act igraphy for 4 nights each; before med ication, dur ingMean age (range or SO) 9.8 (6 .9-12.3) Matched on sex, age. SES med ication. dur ing placebo

Palm e t al., 1992No. of males and females 2 F. 8 M 9F.9 M • Polysomn ographs at home for 2 night sMean age (range or SO) 9.3 (6.3-12.3) 10.7 (8.8-12.6) • No rmal sleeping routines

• No~t fo r adaprionMSl: in lab after 2 night s of record ing

Ramos Platon er al.• 1990No. of males and females 4 F, 9M 43 (no rmative data ) • Polysomnographs in lab for 2 nigh tsMean age (range or SO) 9.0 (6.9-12.1) NA (6-12) • Sleep ad lib, no naps allowed

• First night allowed for adaptionBusby & Pivik, 198 5

No . of males and females 16M 8 M • Polysomnog raph in lab for 4 consecuti ve nightsMean age (range or SO ) 11.0 (1.4) 10.4 (2.0) • First night allowed for adaption

G reenhill et al., 1983No. of males and females 9M 7 F. 4 M • Polysomn01raphs in lab for 2 night s each; baseline (afterMean age (range or SO) 8.6 (6 .7-10.7) 9.3 (8.3-11.8) 2-week was out) . follow-up (6 mon ths from baseline)

• No adap tion night . ad lib sleep schedulePerrino er al., 1983

No. of males and females 12M 12M • Act igr aph y dat a were collected co nti nuo usly fo r aMean age (range or SO) 8.6 (1 .9) 8.6 (2.1) l -week per iod

Poi tras et al., 198 1No. of males and females 4 M 4 M • Polysomnog raphs for 5 nights in labMean "je (range o r SO) NA (8-12) NA (8-12) • First 2 nigh ts allowed for adapr ion

Busby et ., 198 1No. of males and females 11M 11M • Polysom nographs for 5 nights in labMean age (range or SO ) 10.6 (1.7) 10.6 ( 1.3) • Total sleep tim e lim ited to 9.5 hour s

• Lights out at 9:30-10:00. napping not allowedStah l er aI., 1979

No. of males and females 5 NA 9 NA • Polysomnographs for 3 or 4 nigh ts in labMean age (range or SO) NA (6-12) NA (6-12) • First night allowed for adaption

Khan & Recht schaffen, 1978No. of males and females 5M 5 M.2F • Polysomnographs for 3 nights in labMean age (range or SO) NA (6.1-8.5) NA (6.7-8.8) • First night allowed for adaption

Nah as & Kryn icki, 1977" • Polysomnographs in hospital for I or 2 nit, ts each rned-No. of males and females 4M "Normative data

Mean age (range Ot SO) 8.4 (8.0-9.5) NA ication condi tion; free. stan. 2 1st day. an withdrawal• First and 2nd nigh t allowed for adaption

H a;.r. er al.• 1974o. of males and females 6M NC: 6M • Polysomnographs in lab for 5 nights

Mean age (range or SO) NA (8.7-1 4.6) (6.5-1 2.0) • First 2 nigh ts allowed for adaption

Feinberg et al., 1974No. of males and females 8M 6 NA • Polysomn ographs in lab for 4 or 5 nightsMean age (range or SO) 8.8 (7.7-10.5) 8.9 (6.7- 10.6) • First night allowed for adaptio n

Small et al., 1971No. of males and females 3M 7 NA • Polysomn ographs as follows: 5 night s rl acebo . 3 nightsMean age (range or SO) 8.2 (7.8-8.1I) 8.4 (4.8-10.9) 5 m~exedri nelll>. 3 nights optim a dose. 3 nights

place• First night allowed for adaption

Medication

All childr en medicat ion-naive at start• MPH 0 .3 to 0.4 mg/kg once a day for 6 days (in

A.M.) and twice a day for 2 days.• "Unrnedicated"

• Med ication -free for at least 1 mo nth

• 8 ADHO children , no medication pr ior to study• 7 ADHO child ren on M PH• 1 ADHO child on pemo line• 6 months on MPH• Given tw ice dai ly• Mean do se = 1.4 mg/ kg

NA

• "Unmedicared"

• "Nonmedicated"

• I child on MPH• I child off medicat ion for 2 weeks• 3 children off medicat ion for 2 years

• 3 of the ADH O gro up were treated with MPH

• No medication 2 1 days prior to sleep assessment• 20 mg of M PH given for 21 days

• Subjects on medication for 2-36 months• Varying adm inistration schedules• Retested after discontinuing medication

• Short- term: 4 children on Dexedrines' for 2-3 weeks• Long-term: 2 child ren on Dexcd rines' , 2 children on

MPH for 4 mon ths to 6 yearsVarying schedules

• Dose of Dexedrine's did not exceed 20 mglday givenin one do se in A.M .

(")

o;:>::l

'"c~

rr:-;

)­r-

'"'"00 Note: AO H O = atte nt ion-deficit/ hyperactiv ity d isorder; NC = normal control group; F = females; M = males; SES = socioeconomic stat us; NA = information no t available; MPH = meth ylphenidate;MSLT = multiple sleep latency tesr,

Page 5: Sleep Disturbances in Children With Attention‐Deficit/Hyperactivity Disorder

studies less well than normal controls (i.e., greater first­night effect). Acrigraphy (Porrino et aI., 1983; Tiroshet aI., 1993) and home polysomnographs (Palm et aI.,1992) may be more ecologically valid and may requiredifferent degrees of adaption compared with polysorn­nographs conducted in the laboratory.

In sleep studies with adults , it is acceptable practiceto allow at least one night to adapt to the laboratoryenvironment. The majority of studies (13/14) that usedpolysomnographs allowed for one adaptation night.However, it is not known whether children requiremore nights for adaption than adults.

Unlike adult sleep studies, sleep research with chil­dren needs to be particularly concerned with a numberof structural variables such as allowing for naps duringthe day, determining when the child will be awakened,ascertaining the time the child will go to bed, and sleeparrangements (e.g., sleeping alone or with others).These structures are usually implemented by parentsand may vary significantly. Changing these structures(e.g., disallowing naps, setting earlier bedtimes) mayhave an impact on the child 's sleep. A number of studiesrequested that the children not be allowed to nap(Busby et aI., 1981; Ramos Platen er al., 1990), whereassome studies tried to maintain regular bedtime/sleeproutines (Palm er al., 1992).

OUTCOME IN SLEEP RESEARCH WITH ADHD

Subjective Measures of Sleep in ADHD Children

Clinical and parental reports indicate that sleep dis­turbances are associated with ADHD (Barkley, 1990).At present, there is no epidemiological evidence of thisassociation. However, a few studies have examined thebase rate of sleep problems in selected clinical samplesof children with ADHD. Parents of 48 unmedicatedADHD children reported that their children had moredifficulty falling asleep (56% versus 23%) and tirednessupon waking (55% versus 27%) than did parents of 30normal children (Trommer et aI., 1988).

Two questionnaire-based studies by Kaplan et ai.(1987) showed that parents of hyperactive preschoolchildren reported more difficulties with their child'ssleep than parents of normally developing children.These results were confirmed in a third study, whensleep diaries identified approximately 25% of childrenin their ADHD group who had more night wakings,shorter daytime naps, but no difference in total sleeptime or sleep onset latency.

}. AM . ACAD. C H I LD ADOL ESC . PSYCHIATRY, 37 :6, JUNE 1998

SLEEP DISTURBANCES IN ADHD

Objective Measures of Sleep in ADHD Children

Comparisons Between ADHD and Normal Controls.The 14 studies that used objective measures of sleep inchildren with ADHD are listed in Table 2. Twelve ofthese studies used polysomnography, and two usedactigraphy. Incidents of parasomnias in the ADHDpopulation have not been systematically evaluated, andtherefore only information concerning dyssomnias ispresented.

Nine studies compared the sleep onset of childrenwith ADHD and that of normal controls: three studiesfound children with ADHD to have longer latencies tosleep onset (Busby and Pivik, 1985; Haig et aI., 1974;Palm et al., 1992); two studies found shorter sleep onsetlatencies (Ramos Platon et al., 1990; Small et aI., 1971);and four studies found no differences between thegroups (Busby et aI., 1981; Feinberg et aI., 1974;Greenhill et aI., 1983; Tirosh er al., 1993). Total sleeptime was measured in 10 studies. Only one study founda trend between the groups, with the ADHD grouphaving longer total sleep time (Ramos Platon et al.,1990). The remaining nine studies found no differencesbetween the ADHD and normal control groups (Busbyet al., 1981; Busby and Pivik, 1985; Feinberg et al.,1974; Greenhill et aI., 1983; Haig et aI., 1974; Khanand Rechtschaffen , 1978; Small er aI., 1971; Stahl et al.,1979; Tirosh et aI., 1993). Sleep efficiency (relativeproportion of time in bed to time asleep) was addressedin eight studies. None of the studies found that theADHD group had better sleep efficiency than normalsubjects. Three studies found worse sleep efficiency(Palm et al., 1992; Ramos Platon et aI., 1990; Stahlet al., 1979), whereas five did not find any differences(Busby et aI., 1981; Feinberg et aI., 1974; Greenhillet aI., 1983; Small et aI., 1971; Tirosh et al., 1993).

Movements during sleep were measured in sixstudies, two of which used actigraphy (Porrino et al.,1983; Tirosh et al., 1993), and the remaining four usedpolysomnographs (Busby et aI., 1981; Greenhill er al.,1983; Nahas and Krynicki, 1977; Small et aI., 1971).Four of these studies found that ADHD subjectsevidenced more movements in sleep than a normalcontrol group (Busby et aI., 1981; Porrino et al., 1983;Small et aI., 1971; Tirosh et aI., 1993). Two studiesfound no difference in the number of movementsbetween the two groups (Greenhill et al., 1983; Nahasand Krynicki, 1977) . Only one study examinedsleepiness in ADHD subjects through the use of the

641

Page 6: Sleep Disturbances in Children With Attention‐Deficit/Hyperactivity Disorder

C'I n.l>- TABLE 2 0N

Results of O bjective Sleep Studies;:0A

Sleep Efficiency! Additional Findings!C

Sleep O nset 3:Autho rs Latency Total Sleep Awakening Movements REM Sleep NR EM Sleep Impact of Medicat ion

(':"I

--lTiros h et aI.. 1993 AO H O= NC AOHO = NC AO H O= NC AOHO > NC NA NA ADHO had shorte r tota l sleep duration :>-

(trend) lower during MPH than baseline or placebo ;-% quiet sleep

Palm ct aI.. 1992 ADHO > NC NA AOHO < N C NA AOHO = NC AOHO= NC Tolerated procedures less well(1st night (1st night No significant di fferences in daytimeonly) only) sleepiness

Ramos Plaron et al., AD HO< NC AOHO > NC AO H O < NC NA ADHO group had AO HOgroup ADD with hyperactivity had greater sleep1990 less total REM. had increased fragmentation and less sleep efficiency

less % of sleep % stage 3. than AD D without hyperactivityin REM , shorter increased SW S,3rd REM period decreased stage I

Busby & Pivik, 1985 AD H O>NC AOHO = NC NA NA NA NA Arousals to auditory stimuli did not differ(night 4 on ly) by group; however, medication subjects

approxi mated those of NCGreenhill et al., 1983 AOHO = NC ADHO= NC AOHO = NC AOHO = NC AOHO group had AO HO = NC M PH associated with delayed sleep onset ,

reduced REM lengthen ed sleep, and changes in REMactivity and sleep variablesdens ity

Por rino et aI., 1983 NA NA NA ADHO> NC NA NA NA(weekdays only)

Poitras et aI.. 1981 NA NA NA NA NA More spindle NAactivity

Bushy et aI., 1981 ADHO = NC AO HD = NC ADHO =NC AOH O > NC ADHO group had AOHO group had Evidence for a 1st night effect for both:>- (trend) longer latency to more stage 2. groups3:: first REM less stage 4. less:>- SWS in firstr;

cycle:>-v Stahl et aI., 1979 NA AO HO = NC ADHO <NC NA ADHO = NC AO HO = NC Growth hormone levels for ADHO groupr; (9-11 yr old were within normal levelsJ: group)r- Khan & Rechtschaffen, NA AD HO = NC NA NA NA AOHO group had Nu mber of spindles dou bled for subjectsv:>- 1978 less spindle treated with MPHC activity0 Nahas & Krynicki, 1977 NA NA NA AO H O = NC ADHO group had AOHO group had No drug effectr-

""' a decrease in more stage 2,C/Or; REM less stage 4,

C/O increase in sleep-< stage changesr;-r- H aig ct al., 1974 ADHO >NC AOHO = NC NA NA ADHO group had AO HO= NC No drug effect

>: a longer latency No effect of medication withdrawal....,to first REM;:0

:< Feinberg er aI.. 1974 ADHO = NC AOHO= NC AOHO = NC NA ADHO = NC NA Medication led to later onset of REM

'" More intense eye movements (trend)'"C' Small et aI., 1971 ADHO <NC AOHD= NC AOHO =NC AOHO > NC ADHO =NC AOHO=NC Dcxedr ine'" prolonged sleep latency and

C delayed first REM onsetZrn Nate: AO HD = an enrion-deficit/hyperactiviry disorder; AD D = attention deficit d isorder; NC = normal cont rol group; NA = information not available; REM = rapid eye movement ; NREM = non -::; rapid eye movement; SWS = slow-wave sleep; MPH = methyl phenidate.'"co

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multiple sleep latency test. Palm et al. (1992) did notfind any statistically significant differences between thetwo groups in the time to fall asleep in the sequence ofdaytime naps; however, more ADHD children were"sleepy" (i.e., three ADHD subjects had very short sleeponset latencies) . The experimental group had receivedthe diagnosis of "deficits in att ention, motor controland perception," which is similar in many ways toADHD but also has some significant differences (e.g.,focu s on motor and perceptual difficulties and notrestlessness and impulsivity).

Sleep architecture parameters that have beeninvestigated in the ADHD population include amountand density of REM sleep, latency to the onset of REMsleep, and percentage of total sleep time in various sleepstages. REM sleep was examined in 9 studies, andNREM sleep was examined in 10studies. Differences inREM sleep were found between ADHD and normalcontrols in five of the nine studies (Busby et al., 1981;Greenhill er al., 1983; Haig et al., 1974; Nahas andKrynicki, 1977; Ramos Platon et al., 1990). Three ofthese studies reported reduced amount of REM sleep inthe ADHD group. Ramos Platen er al. (1990) foundthat reduced REM was associated with the hyperactivitycomponent of ADHD rather than the inattentioncomponent, and they interpreted this finding as relatingto the instability of ADHD children's sleep. The othertwo studies reported a longer latency to the first REMperiod in the ADHD group. A similar pattern ofinconsistencies was found when NREM was examined.Two studies were specifically designed to measure EEGsleep spindle activity (13 to 15 Hz) , which is thought tobe an index of motor inhibition. One study found areduced number of spindles (Khan and Rechtschaffen,1978), whereas the other study found an increase in thenumber of spindles (Poitras et al., 1981). An additionaleight studies examined other aspects of NREM sleep.Five of these studies found no differences (Greenhillet al., 1983; Haig et a1., 1974; Palm et a1., 1992; Smallet a1. , 1971; Stahl et a1. , 1979) . Two studies foundincreases in stage 2 sleep (Busby et al., 1981; Nahas andKrynicki , 1977), and one found an increase in stage 3sleep for the ADHD group (Ramos Platon et al., 1990).

Stimulant Effiets on Sleep. Eight of the 14 studiesusing objective measures also examined the impact ofstimulant medication (primarily methylphenidate) onchildren with ADHD. Two studies found no differencebetween the no medication and medication conditions

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SLEEP DISTURB ANCES IN ADHD

(Haig et al., 1974; Nahas and Krynicki, 1977). Theremaining six studies did find some differences,although these differences were not considered to be inthe pathological range (Busby and Pivik, 1985; Feinberget a1., 1974; Greenhill et al . , 1983; Khan andRechtschaffen ; 1978; Small et al., 1971; Tirosh et al.,1993). In the study by Khan and Rechtschaffen (1978),the number of spindles doubled after administration ofmethylphenidate. In a study exploring awakening toauditory stimuli (Busby and Pivik, 1985), the ADHDchildren who were taking medication (seven childrentaking methylphenidate and one taking pemoline) weremore like the normal controls than were the nonmedi­cared ADHD children, in that they were more difficultto arouse. This finding was interpreted as potentialsupport for a hyperarousal theory of ADHD. Reducedlatency of sleep onset was noted in one study (Tirosher al., 1993), whereas prolonged sleep onset was foundin another (Small et al., 1971). Three studies notedsome change in REM sleep. Greenhill et al. (1983)found an increased number of REM periods, as well asincreased REM activity and fragmentation. The othertwo studies found a later onset to the first REM period(Feinberg er al., 1974; Small et al., 1971).

The literature search revealed three additional studieswh ich addressed the impact of stimulants on sleep inchildren with ADHD; however, these did not includebaseline comparison with normal controls. Two studiescompared the impact of b.i.d. (two doses a day) andt.i.d. (three doses a day) medication schedules on sleepin children with ADHD. Kent ct a1. (1995) found thata third dose of medication did not change sleep onset(according to nurses' ratings) but did affect level oftiredness upon waking (i.e., children on a t.i.d. schedulewere rated as more tired). Stein er a1. (1996), whoexamined both parent ratings and actigraphy, found thata r.i.d. schedule did not affect sleep duration more thana b.i.d. schedule. However, there was a trend toward areduction in total sleep time on the r.i.d . schedule.Charoor et al. (1983) examined the effect of a noctur­nally administered dose of stimulant medication. Theyfound significant changes in sleep architecture (e.g.,delay in first REM period and a decreased percentage ofREM sleep).

Intervention Research Focused on Sleep and ADHD

The literature search revealed two published casestudies of children with ADHD and a sleep disorder. In

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CORKUM ET AL.

a case study by Dahl et al. (1991), a lO-year-old girlwith ADHD and delayed sleep phase insomnia wastreated with a combination of behavioral modificationand chronorherapy (successively delay sleep timesaround the clock until sleep onset realigns with anearlier clock time) for her sleep disorder. This interven­tion resulted in significant improvements in sleepbehaviors as well as daytime behaviors (e.g., improvedpeer interactions, increased productivity in arithmetictasks, and more completion of seat work). These gainswere maintained over the 4-month follow-up period, asindicated by teacher ratings and classroom perform­ance. Another case study by Bergman (1976) reported abehavioral intervention targeted at insomnia in a 7­year-old boy with ADHD. Elimination of sleep diffi­culties were obtained as well as marked reduction inhyperactivity, and these affects were still evident atfollow-up 6 months later.

The overlap between a diagnosis of sleep disordersand ADHD has led to a number of case studies inwhich "misdiagnosis" of ADHD in children with sleepdisorders has been reported. For example, Hickey et al.(1992) described three children with restless leg syn­drome whose condition had been misdiagnosed asADHD. Picchietti and Walters (1994) found that 34%of children being evaluated for ADHD had sufficientsymptoms of periodic leg movement disorder (PLMD)to warrant a sleep investigation. Of the 34 childrenreferred for a sleep study, 14 had sufficient symptoms tomake a diagnosis of PLMD. This works out to be 20%of the original sample. Treatment for PLMD (clonidineor levodopa/carbidopa) proved successful in treatingboth the nighttime and daytime behavioral difficultiesof these children.

A recent study by Ali er al. (1996) compared childrenwith and without sleep disorders who were on a waitinglist for adenotonsillectomy. After the surgical procedure,the group with sleep disorders displayed significantimprovements in parents' ratings of aggression, inatten­tion, and hyperactivity. They also demonstrated improve­ments on a measure of sustained attention.

Pharmacological interventions for stimulant-inducedsleep disturbances have recently been explored. In anopen study of 18 stimulant-treated ADHD children,Brown and Gammon (1992) found that clonidine (ana-adrenergic agonist) was effective in reducing dif­ficulties with sleep onset. Prince et al. (1996) conducteda retrospective study of 62 children and adolescents with

644

ADHD who had been given clonidine for sleep prob­lems. Sleep problems that were induced or exacerbatedby medication, as well as preexisting sleep problems, allresponded well to the introduction of clonidine (85% ofpatients demonstrated marked improvements) .

Box-Score Interpretation

Parents of ADHD children more often report avariety of sleep problems than do parents of normalcontrols (Kaplan et al., 1987; Trommer et al., 1988). Anestimate of the prevalence of sleep problems based onthese two samples of children with ADHD (total sampleof 113) is between 25% and 50%, compared with 7% ofnormal controls. This represents approximately afivefold increase in the rate of sleep problems in chil­dren with ADHD. Given this finding, it is unlikely thatthe relationship between ADHD and sleep problems isspurious. On the basis of the current research literature,it is impossible to determine whether increased parentalreports of sleep problems in ADHD are unique toADHD or whether they reflect general psychologicaldisturbances. No study has compared sleep disturbancesin ADHD children with those in other pathologicalcomparison groups, nor has any study examined thecontribution of psychosocial factors to the developmentand maintenance of sleep problems in this population.

The results of the studies that used objective mea­sures of sleep were often inconsistent. In eight of thestudies that assessed sleep onset latency, it was found tobe longer (33%), shorter (22%), and the same (45%). Afairly consistent result was evident across studies fortotal sleep time, with 90% of the studies (9110) findingno difference between children with ADHD andnormal controls. Sleep efficiency was significantly lessfor the ADHD group in 38% of the studies (3/7) anddid not differ in the remaining studies. Sixty-sevenpercent of the studies (4/6) found that the ADHDgroup displayed more movements during sleep. Anequal number of studies found differences between theADHD group and normal control group in REM andNREM sleep as those that did not find differences(REM and NREM: 55% and 50% found differences,respectively).

Because sample sizes were very small, the inconsistentfindings may reflect type II errors (chance occurrence ofstatistically significant findings) or may reflect inade­quate and inconsistently applied diagnostic criteria forADHD. Only two relatively consistent findings across

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the studies were found. First, the ADHD group did notdiffer from the normal control group on total sleep time(90% of studies found no difference). This finding isalso consistent with the studies that used subjectivemeasures. Second, children with ADHD were found tobe more restless during sleep (67%). Actigraphy seemedmore sensitive to these differences than polysomno­graphic readings, with both of the studies using actig­raphy finding differences compared with half of thestudies that used polysomnographs.

Changes in various sleep parameters with the intro­duction of stimulant medication were noted in 75% ofthe studies (6/8). Typically, stimulant medicationprolonged sleep latency and onset to first REM cycle;however, these changes were not considered to place thechild in the "pathological" range indicative of a serioussleep disorder. Control procedures make interpretationof this finding difficult given that children were takingdifferent medications at different doses and adhering todifferent administration schedules. Also, many of thechildren were not medication-naive and went throughvarying lengths of "washout" periods prior to participat­ing in the sleep studies.

CLINICAL IMPLICATIONS

Clinically it would appear prudent to assess childrenwith ADHD for sleep disturbances. Sleep problems inchildren have been reported as a significant stressor forparents (Saxby and Morgan, 1993), yet they are rarelymentioned in clinical interviews. Anecdotal reportssuggest that treatment for specific sleep problemsimproves attention and hyperactivity, as well as familyfunctioning, and reduces stress levels. Even though thereason and nature of sleep disturbances in ADHDremain unknown, behavioral treatment of these diffi­culties may provide symptom relief for children withADHD and improvement in their family relationships.

CONCLUSIONS

This review highlights the importance of futureinvestigations of the relationship between ADHD andsleep disorders. Future studies should (l) provideprecise characterization of the type, severity, frequency,and significance of sleep problems in children who havea confirmed diagnosis of ADHD; (2) compare sleepparameters of children with ADHD with those of bothnondisabled children and other children with behaviorproblems, learning disabilities, and sleep disturbances;

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(3) explore the impact of comorbid disorders (e.g.,anxiety) on the presentation of sleep disturbances inchildren with ADHD; and (4) determine the reason forthe apparent contradictory findings between studiesusing subjective and objective methodologies (for a dis­cussion of this issue see Ball and Koloian, 1995).Finally, the inference that stimulant medication doesnot have a detrimental impact on sleep in children withADHD (Ball and Koloian, 1995) should be reviewedfurther given recent findings that sleep problems persistwith extended treatment of ADHD with stimulantmedication (Schachar et al., 1996).

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Clinical Perspectives in Primary Nocturnal Enuresis. G retc hen A. Gimpel . PhD. W illiam] . Warzak. PhD. Brett R. Kuhn. PhD.

John N . Walburn. MD

Primary nocturnal enu resis (PN E) is prevalent among th e ped iatr ic populat ion . but not all professionals are aware of the current

research regarding th e et iology and treatment of this disorder. This paper p resents a broad overview of PNE, including etiologyand evaluatio n, with a specific emphasis on treatment issues. The most curr ent trea tments (imi p ram ine, desmopressin acet ateargini ne vasopressin . enuresis alarm s) are disc ussed . inclu d ing recent research on their effect iveness. In consideri ng the recent datao n long-term efficacy, overall cos t. and safety, th e treatment of choice appears to be th e enuresis alarm for those famil ies who arecapable of follow ing protocols . D esmopressin acetate argini ne vasopressin is a safe alternative that has the adva nta ge of quickresponse and ease of ad m inistratio n. Clin Pediatr 1998;37:2 3-30

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