Parental Symptom Report and Periodic Limb Movements of Sleep in Children
Bradley T. Martin, MB.BS., FRACP,1 Bruce D. Williamson, B.Sc.,2 Natalie Edwards, Ph.D.,3 and Arthur Y Teng, MB.BS.4
1Department of Sleep Medicine, Sydney Children’s Hospital, Randwick, NSW, Australia; School of Women’s and Children’s Health, University of New South Wales, NSW, Australia
2Department of Sleep Medicine, Sydney Children’s Hospital, Randwick, NSW, Australia
3Department of Sleep Medicine, Sydney Children’s Hospital, Randwick, NSW, Australia; Department of Medicine, University of Sydney, Australia
4Department of Sleep Medicine, Sydney Children’s Hospital, Randwick, NSW, Australia; School of Women’s and Children’s Health, University of New South Wales, NSW, Australia
Address correspondence to: Dr. Bradley T Martin, Department of Sleep Medicine, Sydney Children’s Hospital, High St, Randwick, NSW, 2031, Australia, Phone: (612) 9382 1210, Fax: (612) 9382 0399, ; Email: btmartin/at/optusnet.com.au
Received May 2007; Accepted October 2007.
To examine the prevalence of raised periodic limb movements of sleep (PLMS) index in children referred for polysomnography (PSG) and whether parental report of symptoms correlates with objective measurement during PSG.
Records of children undergoing PSG from January 2006 to July 2006 were retrospectively reviewed. At their initial sleep clinic visit, parents had been asked whether their child was restless or moved their legs excessively during sleep. Their response to these questions was compared to the child’s PLMS index (number of periodic limb movements per hour) during a full PSG. PLMS were scored according to internationally accepted criteria.
Data were examined for 101 children (60 male) with mean age 6.5 years (range 1.2 to 17.6 years). Excessive leg movements were reported by parents in 50% and restlessness in 73%. A raised PLMS index (defined as >5 per hour) was noted in 10 cases (prevalence 10%). Asking parents about whether their child kicks their legs excessively in sleep had sensitivity 50%, specificity 51%, positive predictive value (PPV) 10%, negative predictive value (NPV) 90% and positive likelihood ratio (LR+) 1.02 when compared to objective analysis. Asking parents about whether their child is restless in sleep had sensitivity 70%, specificity 26%, PPV 9%, NPV 89% and LR+ 0.95.
Asking parents about their child’s symptoms is not an accurate predictor of raised PLMS index. We recommend that leg electromyography be used in all pediatric sleep studies to record PLMS.
Martin BT; Williamson BD; Edwards N; Teng AY. Parental symptom report and periodic limb movements of sleep in children. J Clin Sleep Med 2008;4(1):57-61.
Keywords: Periodic limb movements of sleep, child, questionnaires, polysomnography, sensitivity and specificity, likelihood ratio
Periodic limb movements of sleep (PLMS) are recognized as stereotyped, repetitive movements of the limbs during sleep. Movements described include extension of the great toe (similar to the Babinski response), flexion of the foot and lower leg or abrupt extension of the lower leg.1 Movements of the upper limbs may also occur. PLMS occur most commonly in light sleep (stage 1 and 2) and are scored according to internationally accepted criteria originally developed by Coleman2 and recently updated by the American Academy of Sleep Medicine.3 An index of 5 or more PLMS per hour is considered abnormal, although data supporting this figure are limited.4 PLMS in children have been associated with iron deficiency,5–7 symptoms of attention deficit hyperactivity disorder (ADHD)8–12 and “growing pains.”1,13
In periodic limb movement disorder (PLMD), a rate of 5 or more PLMS per hour is accompanied by clinical sleep disturbance with a further diagnostic criterion that the leg movements cannot be accounted for by sleep disordered breathing (SDB) or medication such as antidepressants.4 The condition may be due to underactive dopaminergic pathways in the central nervous system.14–16 PLMD is a well-recognized but controversial phenomenon in adults but is thought to be under-recognized in children.17 PLMS index >5 has been noted to be uncommon in children and adolescents compared to adults aged >40 years.18 A large European survey reported a prevalence of 3.9% in the general population including 3.2% in adolescents aged 15 to 19 years, but polysomnography (PSG) data did not form part of the study.19 Studies including PSG have quoted prevalence in children ranging from 5.6% to 26% in several general and referred populations.10,17,20,21
Restless legs syndrome (RLS), which can be considered a separate but related condition to PLMD, is diagnosed clinically by the presence of uncomfortable sensations in the legs which tend to be worse in the evening or night and are relieved by movement. Most people with PLMS do not have clinical symptoms of RLS but up to 80% of RLS sufferers have significant PLMS noted during PSG.22 PLMS do not form part of the essential diagnostic criteria for RLS but they do provide supportive evidence.4
The prevalence of PLMS in children is not well defined23 and symptoms are often not well reported by children or their parents. Furthermore, PLMS are not routinely recorded and scored in all pediatric sleep laboratories. We sought to examine the prevalence of raised PLMS index in a population of children referred for PSG. We also examined whether parental report of symptoms predicted presence of PLMS on objective measurement. To limit confusion among PLMS, PLMD, and RLS, which often arises in the literature, we primarily examined PLMS as a PSG finding rather than PLMD or RLS as clinical disorders.
Records of children who underwent PSG at Sydney Children’s Hospital, Randwick, NSW, Australia between January and July 2006 were examined. At their initial clinic appointment with one of the authors (AYT), a standard questionnaire had been administered. This included asking parents whether their child was restless or moved their legs excessively during sleep. From the patient records, data were obtained for the following parameters: age; sex; indication for PSG; parental report of restlessness in sleep; parental report of excessive leg movements in sleep; PLMS index (number of PLMS per hour); and mixed/obstructive apnea/hypopnea index (MOAHI: number of mixed or obstructive apneas and hypopneas per hour of sleep). Children were excluded if they were younger than one year of age, did not have a complete diagnostic PSG, or had a neuromuscular or severe neurodevelopmental condition which could interfere with estimation of PLMS. We included studies supervised by a single physician to ensure consistency in questioning about symptoms.
PSG was performed using Compumedics S or E Series (Compumedics, Melbourne, Australia). Studies were scored by the authors according to the criteria of Rechtschaffen and Kales.24 Sleep stages were scored manually using electroencephalography, electro-oculography, and submental electromyography (EMG). Audio and video were digitally recorded. Respiratory efforts were measured by respiratory bands as well as EMG of diaphragm and abdominal muscles. Nasal airflow was recorded using nasal cannulae with a pressure transducer and oronasal flow was measured by thermistor. Oxygen saturation (SpO2) was measured by pulse oximetry (Nellcor 595, Nellcor Puritan Bennett, Pleasanton, CA, USA) and electrocardiogram was recorded continuously. Carbon dioxide was recorded continuously by a transcutaneous electrode (Radiometer, Copenhagen, Denmark). Bilateral anterior tibialis EMG signals were calibrated at commencement of recording by voluntary movement in older children and as part of general calibration in younger children.
Respiratory Event Scoring
Central apnea was defined as cessation of airflow and effort for two or more respiratory cycles with SpO2 decrease of >3% from baseline. Obstructive apnea was defined as cessation of oronasal airflow with continuing respiratory effort regardless of SpO2. Hypopnea was defined as airflow 20% to 50% of baseline amplitude and as central or obstructive according to associated absence or presence of respiratory effort. Events with both central and obstructive components were scored as mixed apneas. MOAHI was calculated as the total number of mixed apneas, obstructive apneas and obstructive hypopneas per hour of sleep. MOAHI ≥1 is considered abnormal in children.25
Periodic limb movements were scored according to accepted criteria as follows: (1) movements 0.5 s to 5 s in duration; (2) interval between movements 5 s to 90 s; (3) ≥4 movements in sequence; (4) movement at least 25% of calibrated magnitude.3 Movements following arousals due to respiratory events were not scored.
Data were compiled in Microsoft Excel (Microsoft Corporation, Redmond, WA, USA) and analysed using SPSS Version 12.0 (SPSS Inc, Chicago, IL, USA). PLMS data were dichotomised into categories of 5 was taking fluoxetine, which may have exacerbated the condition.26 Parents of this child had reported both restlessness and excessive leg movements in sleep. This child was also the only one of the 10 with raised PLMS index to have reported “growing pains.”
Association of PLMS with Symptoms
Excessive leg movements in sleep were reported by 50 parents (50%) and restlessness was reported by 74 parents (73%). Parental report rate was significantly higher than the rate obtained by objective recording for excessive leg movements (McNemar χ21df = 30.4, p < 0.001) and for restlessness (McNemar χ21df = 56.7, p 5 of 10% in our referred population is similar to that reported by Crabtree et al of 11.9% in a community sample (χ21df = 0.33; p = 0.57) and 8.4% in a referred population (χ21df = 0.24; p = 0.63).17 It is also not statistically different from the rate of 5.6% reported by Kirk and Bohn in a referred population (χ21df = 2.76; p = 0.10).20 Traegar et al performed PSG on a group of children specifically excluding those likely to have OSA and reported a similar rate to ours of 8% (χ21df = 0.26; p = 0.61).21 Our rate, however, was lower than the 26% reported by Chervin and Archbold in children referred for suspected sleep disordered breathing (χ21df = 8.89; p = 0.003).10 Chervin and Archbold used slightly broader criteria for scoring PLMS (periodicity of 5 s to 120 s and sequence ≥3 movements), which may have resulted in more children being classified with raised PLMS index. It is important to note, however, that study populations and referral patterns are likely to have differed between the above studies so it is difficult to draw firm conclusions from these comparisons.
Chervin et al examined symptoms useful in predicting PLMD in order to compile a questionnaire.13 Asking about restlessness of the legs, growing pains in bed, insomnia, and morning headache were moderately predictive; but questions about leg movements during sleep, daytime sleepiness, and daytime behavior were not. Overall sensitivity and specificity of the final questionnaire based on symptoms associated with PLMS ≥5 per hour were only 79% and 56% respectively. Receiver-operator analysis suggested only moderate utility of their PLMS score as a diagnostic tool. This implies, as does our study, that clinical suspicion cannot be relied upon in the diagnosis of PLMS.
Martinez and Guilleminault noted that the report of leg pains at morning waking was associated with PLMS of any degree but that other symptoms such as sleep initiation problems, sleep maintenance problems, and daytime tiredness were not specific.1 Reporting of leg pains had sensitivity 80% and specificity 82% and may be a more useful symptom about which to enquire than leg movements in sleep or restlessness, although only one of the 10 subjects with raised PLMS index in our study reported such pain.
Picchietti and Walters, in a study of 129 children with PLMS index >5, reported that parents had noted the presence of PLMS in only 25 cases (19%), and even after being asked to look for leg movements did not notice them in 39 cases (30%).27 Furthermore, symptoms were only reported in 3 of 16 children considered severe cases with PLMS index >25. Another study noted substantial disparity between parental symptom report and PLMS index in a study of children with ADHD.9 Crabtree also noted no significant difference in reported symptoms by parents of children with and without PLMD,17 again highlighting the difficulty in using parental reports for diagnosis.
PLMD is an important diagnosis to consider as patients may be misdiagnosed with conditions such as ADHD and seizures if the diagnosis is not considered.26 Normal phenomena such as body shifts, hypnic jerks and phasic REM twitches may also be misinterpreted as PLMS.9 The condition is also potentially treatable, particularly if associated with SDB or low ferritin levels.1 Unfortunately, we were not able to perform repeat PSG on all of our patients to examine the effect of treatments such as adenotonsillectomy, CPAP, or iron therapy on PLMS index.
Six of the 10 subjects with raised PLMS index in our study also showed evidence of SDB. As leg movements directly following arousal due to respiratory events were not scored, we feel that PLMS can be considered a separate but perhaps related phenomenon in these children. Kirk and Bohn20 (60%), and Martinez and Guilleminault1 (50%) have reported similar comorbidity rates. Martinez and Guilleminault noted similar rates of SDB in children with and without PLMs, again implying independence of the conditions. They also noted that in 15 of 29 comorbid children treated for SDB, PLMs also resolved, but PLMs persisted or increased in the others.1 Chervin and Archbold found that PLMS index was related to hyperactivity scores in children with SDB—but not those without—and hypothesized that SDB may act as an effect modifier of PLMS.10 These and other studies highlight the difficulty in assessing the relationship between PLMS and SDB and the necessity to exclude movements associated with SDB-related arousals from scoring of PLMS. Regarding other comorbidities, none of our subjects was diagnosed with narcolepsy or REM sleep behavior disorder; these disorders are also commonly associated with PLMS. As data were not available for specific symptoms of RLS, we were not able to assess accurately the presence of this associated condition in our study sample.
PSG is widely recognized as the gold standard for diagnosis of PLMS as well as many other sleep disorders, but its complexity and expense limit its use in many environments. Actigraphy has been assessed as a more economical, less labor-intensive alternative method of diagnosis, but results have been conflicting.28–30 PSG, therefore, remains essential in the recording of PLMS.
As this was a retrospective study, PSGs had been reported in a clinical context and hence the reporter was not necessarily blinded to the symptom reports of the parents. We feel, however, that the use of standard, validated criteria to score PLMS counterbalanced this potential bias. Our sample size was based on pragmatic considerations, but we feel it compares well with other studies on this topic. Our use of a population referred for investigation of sleep problems, primarily snoring, also means that our results cannot be extrapolated to the general population but should be relevant for the practice of sleep medicine in most pediatric units.
Parental report of excessive leg movements or restlessness in sleep is not an accurate predictor of raised PLMS index compared with objective measurement during PSG. A negative report of symptoms is fairly likely to exclude significant PLMS but overall these symptoms perform poorly as diagnostic tools. As PLMS represent a potentially treatable condition in children which is associated with significant comorbidities, we recommend objective scoring of PLMS during PSG for all children over the age of one year.
1. Martinez S, Guilleminault C. Periodic leg movements in prepubertal children with sleep disturbance. Dev Med Child Neurol. 2004;46:765–70. [PubMed]
2. Coleman RM, Pollak CP, Weitzman ED. Periodic movements in sleep (nocturnal myoclonus): relation to sleep disorders. Ann Neurol. 1980;8:416–21. [PubMed]
3. American Academy of Sleep Medicine. International classification of sleep disorders, second edition: Diagnostic and coding manual. Westchester, IL: American Academy of Sleep Medicine; 2005.
4. Allen RP, Picchietti D, Hening WA, Trenkwalder C, Walters AS, Montplaisir J. Restless legs syndrome: diagnostic criteria, special considerations, and epidemiology. A report from the restless legs syndrome diagnosis and epidemiology workshop at the National Institutes of Health. Sleep Med. 2003;4:101–19. [PubMed]
5. Kryger MH, Otake K, Foerster J. Low body stores of iron and restless legs syndrome: a correctable cause of insomnia in adolescents and teenagers. Sleep Med. 2002;3:127–32. [PubMed]
6. Simakajornboon N, Gozal D, Vlasic V, Mack C, Sharon D, McGinley BM. Periodic limb movements in sleep and iron status in children. Sleep. 2003;26:735–8. [PubMed]
7. Kotagal S, Silber MH. Childhood-onset restless legs syndrome. Ann Neurol. 2004;56:803–7. [PubMed]
8. Picchietti DL, England SJ, Walters AS, Willis K, Verrico T. Periodic limb movement disorder and restless legs syndrome in children with attention-deficit hyperactivity disorder. J Child Neurol. 1998;13:588–94. [PubMed]
9. Picchietti DL, Underwood DJ, Farris WA, et al. Further studies on periodic limb movement disorder and restless legs syndrome in children with attention-deficit hyperactivity disorder. Mov Disord. 1999;14:1000–7. [PubMed]
10. Chervin RD, Archbold KH. Hyperactivity and polysomnographic findings in children evaluated for sleep-disordered breathing. Sleep. 2001;24:313–20. [PubMed]
11. Chervin RD, Archbold KH, Dillon JE, et al. Associations between symptoms of inattention, hyperactivity, restless legs, and periodic leg movements. Sleep. 2002;25:213–8. [PubMed]
12. Cortese S, Konofal E, Lecendreux M, et al. Restless legs syndrome and attention-deficit/hyperactivity disorder: a review of the literature. Sleep. 2005;28:1007–13. [PubMed]
13. Chervin RD, Hedger KM. Clinical prediction of periodic leg movements during sleep in children. Sleep Med. 2001;2:501–10. [PubMed]
14. Staedt J, Stoppe G, Kogler A, et al. Nocturnal myoclonus syndrome (periodic movements in sleep) related to central dopamine D2-receptor alteration. Eur Arch Psychiatry Clin Neurosci. 1995;245:8–10. [PubMed]
15. Turjanski N, Lees AJ, Brooks DJ. Striatal dopaminergic function in restless legs syndrome: 18F-dopa and 11C-raclopride PET studies. Neurology. 1999;52:932–7. [PubMed]
16. Ruottinen HM, Partinen M, Hublin C, et al. An FDOPA PET study in patients with periodic limb movement disorder and restless legs syndrome. Neurology. 2000;54:502–4. [PubMed]
17. Crabtree VM, Ivanenko A, O’Brien LM, Gozal D. Periodic limb movement disorder of sleep in children. J Sleep Res. 2003;12:73–81. [PubMed]
18. Pennestri MH, Whittom S, Adam B, Petit D, Carrier J, Montplaisir J. PLMS and PLMW in healthy subjects as a function of age: prevalence and interval distribution. Sleep. 2006;29:1183–7. [PubMed]
19. Ohayon MM, Roth T. Prevalence of restless legs syndrome and periodic limb movement disorder in the general population. J Psychosom Res. 2002;53:547–54. [PubMed]
20. Kirk VG, Bohn S. Periodic limb movements in children: prevalence in a referred population. Sleep. 2004;27:313–5. [PubMed]
21. Traegar N, Scgultz B, Pollock AN, Mason T, Marcus CL, Arens R. Polysomnographic values in children 2-9 years old: additional data and review of the literature. Pediatr Pulmonol. 2005;40:22–30. [PubMed]
22. Montplaisir J, Boucher S, Poirier G, Lavigne G, Lapierre O, Lesperance P. Clinical, polysomnographic, and genetic characteristics of restless legs syndrome: a study of 133 patients diagnosed with new standard criteria. Mov Disord. 1997;12:61–5. [PubMed]
23. Simakajornboon N. Periodic limb movement disorder in children. Paediatr Respir Rev. 2006;7(Suppl 1):S55–7. [PubMed]
24. Rechtschaffen A, Kales A. A manual of standardized terminology, techniques and scoring systems for sleep stages of human subjects. Washington, DC: National Institutes of Health; 1968.
25. Marcus CL, Omlin KJ, Basinki DJ, et al. Normal polysomnographic values for children and adolescents. Am Rev Respir Dis. 1992;146:1235–9. [PubMed]
26. Dorsey CM, Lukas SE, Cunningham SL. Fluoxetine-induced sleep disturbance in depressed patients. Neuropsychopharmacology. 1996;14:437–42. [PubMed]
27. Picchietti DL, Walters AS. Moderate to severe periodic limb movement disorder in childhood and adolescence. Sleep. 1999;22:297–300. [PubMed]
28. Shochat T, Oksenberg A, Hadas N, Molotsky A, Lavie P. The KickStrip: a novel testing device for periodic limb movement disorder. Sleep. 2003;26:480–3. [PubMed]
29. King MA, Jaffre MO, Morrish E, Shneerson JM, Smith IE. The validation of a new actigraphy system for the measurement of periodic leg movements in sleep. Sleep Med. 2005;6:507–13. [PubMed]
30. Montgomery-Downs HE, Crabtree VM, Gozal D. Actigraphic recordings in quantification of periodic leg movements during sleep in children. Sleep Med. 2005;6:325–32. [PubMed]
Dr Widodo Judarwanto SpA
CHILDREN SLEEP CLINIC
Powered by blacberry messanger