Migraine and periodic limb movement disorders in sleep in children: a preliminary case–control study
© Esposito et al.; licensee Springer. 2013
Received: 16 April 2013
Accepted: 22 June 2013
Published: 1 July 2013
The relationships between sleep and headaches are complex and manifold. About the variety of phenomena that can disrupt the sleep macrostructure and can impact its restorative function, the periodic limb movements disorder (PLMd) can be considered as the most powerful.
No studies are known about the role of PLMd in the pathophysiology of migraine in children.
Aim of study is to assess the prevalence of PLMd and migraine and their relationship with disability and pain intensity in a pediatric sample, referred for migraine without aura by pediatricians.
After a preliminary sleep habits screening with the Sleep Disturbances Scale for Children, 34 migraine subjects affected by migraine without aura (20 M, 14 F) (mean age 9.08; SD ± 2.28) and 51 volunteers healthy children (28 M, 23 F) (mean age 9.37; SD ± 1.81) accepted to underwent overnight PSG recordings in the Sleep Laboratory of the Clinic of Child and Adolescent Neuropsychiatry, in order to define the macrostructural sleep characteristics and the prevalence of PLMd. Subsequently, the migraineurs sample was studied in order to define the relationship between disability, pain intensity, therapeutical responsiveness and the presence of PLMd.
In the migraineurs children group, the individuals with PLM pathological index (PLMI ≥ 5) represent the 26.47% of sample and present higher frequency (p < 0.001), intensity (p < 0.001), duration (p = 0.006) and life impairment as scored in the PedMIDAS (p < 0.001) of headache and lower efficacy of prophylactic (p = 0.001) and acute (p = 0.006) pharmacological treatment than MoA children without PLM pathological index.
This preliminary study indicates the potential value of the determination of the PLMd signs, and the importance of the PSG evaluation in children affected by migraine, particularly when the clinical and pharmacological management tend to fail in the attacks control.
KeywordsPolysomnography Periodic limb movements PLMd PLMs Children Migraine without aura MoA
The relationships between sleep and headaches are complex and manifold [1, 2], with suggestions for an unique pathogenic process . Among the causes of disturbed sleep in subjects affected by primary headache, the sleep apnea syndrome and the restless legs syndrome (RLS) were considered yet in 1990 by Sahota and Dexter .
In particular, RLS is a sensorimotor disorder characterized by an irresistible urge to move the limbs predominantly in the evening or at night, usually accompanied by a peculiar discomfort in the lower extremities often alluded to as a “creepy” or “crawly” feeling, with insomnia and daytime fatigue as a consequence [5, 6]. The nocturnal polysomnography (PSG) may show the association of periodic limb movement disorder (PLMd) during the night.
According to the International Classification of Sleep Disorders - 2nd Edition (ICSD-2) criteria, Periodic Limb Movement Disorder (PLMd) is caused by periodic episodes of repetitive, highly stereotyped, limb movements that occur during sleep, with a frequency >15/h (in children >5/h), associated with a clinical sleep disturbance or a complaint of daytime fatigue .
Specifically, a leg movement is classified as PLM if it is part of a periodic sequence of leg movements which involve the rhythmic extension of the big toe and dorsiflexion of the ankle, occasionally accompanied by knee and hip flexion. By definition, periodic limb movements are not the result of generalized neurological disorders, which are typically apparent during wakefulness as well as during sleep , and defined as four or more consecutive leg movements with a duration of 0.5-10 s, with an EMG increase of >8 μV above the resting baseline, and a minimum interval of 5 s and a maximum of 90 s between two consecutive leg movements [9, 10].
Although the effects of PLMd have been well studied in adults, there have been limited and scarce reports in developmental age, associated with transient arousals and sleep fragmentation, which could lead to changes in daytime neurocognitive and behavioral patterns .
In children, the presence of PLMd may be frequently associated with low serum iron and with a tendency toward low serum ferritin levels .
Moreover, more conditions such as obstructive sleep apnea syndrome (OSAS), autism, ADHD, Williams syndrome, Tourette syndrome, narcolepsy, and medications like selective serotonin reuptake inhibitors, lithium and tricyclic antidepressants can be considered as risk factors for PLMd . Since the description in adults in the 1980’s, their prevalence in children and adolescents is still unclear. Reported prevalence rates of the PLMd a frequency at least of 5/hr vary between 1.2% to 10% of children not referred specifically for PLMd or restless legs syndrome (RLS) [15, 16], while the prevalence in children with migraine is largely unknown. Chervin and Hedger  reported that restlessness of the legs, growing pains in bed, insomnia, and morning headache can be considered as moderately predictive value for the identification of paediatric PLMd.
To our knowledge, there are no data about the relationship between PLMd and migraine in developmental age, and the putative common mechanisms underlying the two conditions.
Therefore, the aim of the present study is to assess the prevalence of PLMd and migraine and their relationship with disability and pain intensity in a pediatric sample of children affected by migraine without aura.
187 children affected by migraine without aura (MoA) (74 F, 113 M) aged 5–17 years, (mean 9.92 ± 2.86) were consecutively referred to the Center for Childhood Headache of Child and Adolescent Neuropsychiatry Clinic at the Second University of Naples, from September 2011 to December 2012. They were all referred from primary care paediatricians.
The diagnosis of MoA was made according to the International Classification of Headache Disorders. 2nd Edition (ICHD-2) .
All mother’s of starting population subjects filled out a questionnaire in order to assess the sleep habits (Sleep Disturbances Scale for Children, SDSC) of their children and compared with a control group composed by 766 typical developing children (342 F, 424 M; mean age 10.05 ± 2.13) comparable for age (p = 0.494) and sex distribution (Chi-square =1.374; p = 0.241), recruited in the Campania Region schools.
Therefore, from original population of 187 migraine children the subjects with SBD referred signs, EEGs abnormalities or epileptic discharges, neuro-anatomical alterations (assessed by RMN and/or TC evaluation) or psychiatric illness (depression, behavioural problems and ADHD) or mental retardation (IQ ≤70) or subjects under treatment with anticonvulsant or psychoactive drugs were excluded.
Finally, only 34 migraine subjects affected by MoA (20 M, 14 F) (mean age 9.08; SD ± 2.28) and 51 volunteers typical developing children (28 M, 23 F) (mean age 9.37; SD ± 1.81) accepted to underwent overnight PSG recordings.
All the subjects were recruited from the same urban area, were all Caucasian origin, and had middle socioeconomic status.
All evaluations were performed after informed parental consent was obtained for all the children enrolled, according to the World Medical Association .
The study was approved by the Departmental Ethics Committee at the Second University of Naples.
In order to exclude the presence of alteration in iron metabolism (low serum iron and low serum ferritin levels), the blood samples for hemoglobin, and iron status evaluations were drawn in the morning (at 08:00 h) after overnight fasting. Hemoglobin was measured in whole blood using an automated Coulter counter, and cut-off points used to define anemia were based on the 5th percentiles for the reference groups .
In particular, the iron status has been assessed by serum iron, transferrin, and ferritin concentrations. Transferrin saturation has been calculated.
In order to exclude subjects with overweight or obesity, weight and height were measured and BMI was calculated. Standard deviations scores for BMI were calculated by using the LMS method .
Sleep habits assessment
To evaluate sleep habits and disturbances, all mother’s of starting population subjects filled out the Sleep Disturbances Scale for Children (SDSC) questionnaire . This is a standardized questionnaire for the assessment of pediatric sleep problems consisting of 26 items grouped into 6 subscales: DIMS (Disorders in Initiating and Maintaining Sleep), SBD (Sleep Breathing Disorders), DA (Disorders of Arousal), SWTD (Sleep-Wake Transition Disorders), DOES (Disorders Of Excessive Somnolence), SHY (Nocturnal Hyperhydrosis). The SDSC questionnaire is widely used in school-aged children both in the original [22, 23] or as modified version .
The results were compared with those obtained by SDSC questionnaires of a control group composed by 766 children (342 F, 424 M; mean age 10.05 ± 2.13) matched for age (p = 0.494) and sex distribution (Chi-square =1.374; p = 0.241), recruited in the Campania region schools.
The subjects of both groups were recruited from the same urban area, were all Caucasian origin, and had middle socioeconomic status.
Polysomnographic sleep recordings
34 migraine subjects affected by MoA (20 M, 14 F) (mean age 9.08; SD ± 2.28) and 51 volunteers healthy children (28 M, 23 F) (mean age 9.37; SD ± 1.81) accepted to underwent overnight PSG recordings in the Sleep Laboratory of the Clinic of Child and Adolescent Neuropsychiatry, after one adaptation night, in order to avoid the “first-night effect”. The groups that underwent PSG were matched for age (p = 0.516), and gender distribution (Chi-square = 0.018; p = 0.893).
As previously reported in other polysomnographic studies [25–28], electroencephalographic (EEG) recordings and electrode placement were performed according to the 10–20 system  and the polysomnographic montage included at least 19 EEG channels (Fp2, Fp1, F3, F4, F7, F8, C3, C4, T3, T4, P3, P4, T5, T6, O1, O2, Fz, Cz, Pz) referenced to the contralateral mastoid, left and right electro-oculogram, chin electromyogram, left and right tibialis electromyogram, electrocardiogram (one derivation), nasal cannula, thorax and abdominal effort, peripheral oxygen saturation, pulse, and position sensors.
The recordings were carried out using a Brain Quick Micromed System 98 recording machine, and signals were sampled at 256 Hz and stored on a hard disk for further analysis. EEG signals were digitally band-pass filtered at 0.1–120 Hz, with 12-bit A/D precision. Sleep signals were sampled at 200 Hz or 256 Hz and stored on a hard disk in European data format for further analysis. EEG signals were first acquired with a wide band analog filter (0.001–70 Hz) and then digitally band-pass filtered at 0.1–50 Hz. All recordings started at the subjects’ usual bedtime and continued until spontaneous morning awakening.
Sleep stage scoring
Sleep was subdivided into 30-second epochs, and sleep stages were scored using standard criteria .
The following conventional sleep parameters were evaluated:
Time in bed
Sleep period time: time from sleep onset to end of sleep
Total sleep time: time from sleep onset to the end of the final sleep epoch minus time awake
Sleep latency: time from lights out to sleep onset, defined as the first of two consecutive epochs of stage 1 sleep or one epoch of any other stage, in minutes
REM latency: time from sleep onset to the first REM sleep epoch
Number of stage shifts/hour
Number of awakenings/hour
Sleep efficiency: percentage ratio between total sleep time and time in bed (total sleep time/time in bed * 100)
Percentage of sleep period time spent in wakefulness after sleep onset, i.e., time spent awake between sleep onset and end of sleep
Percentage of sleep period time spent in sleep stages 1 (S1%) and 2 (S2%), slow-wave sleep (SWS%), and REM sleep (REM%)
All variables were analyzed by Hypnolab 1.2 sleep software analysis (SWS Soft, Troina, Italy). All recordings were visually scored by one of the investigators (MC), and the sleep parameters derived were tabulated for statistical analysis.
In order to exclude the presence of sleep-related breathing disorders, nocturnal respiratory parameters (i.e., central, obstructive, and mixed apnea events) were counted using standard criteria .
Standard criteria were used to identify episodes of periodic limb movements. The frequency of leg movements was represented as the periodic leg movement index (number/hour of total sleep time). Episodes of periodic limb movements were defined as leg movements with an amplitude increase of 8 μV above the baseline value, a duration of 0.5–10 seconds, a period length between two consecutive movements of 5–90 seconds, and a minimum of four consecutive movements . A periodic leg movement index ≥ 5 was considered abnormal.
In the MoA group, in order to compare the headache characteristics between children with PLMd and children without PLMd (no-PLMd), we take in account the MoA frequency and the duration of headache attacks per month, the pain intensity (VAS index), the PedMIDAS score, and the subjective response to the pharmacological treatment such as acute treatment (i.e.: Paracetamol efficacy) and prophylactic treatment (Preventive therapy efficacy; i.e.: Flunarizine) obtained by the clinical interview.
The visual analogue scale (VAS) was used to assess the level of pain, by placing a mark on an horizontal line 10-cm long at an appropriate distance between the two endpoints (no pain signed as happy smiley and most intense pain imaginable signed as hopeless smiley).
The PedMIDAS is a sensitive, six-question interview that can be easily administered by both parent and child to assess the impact of recurrent headaches on a child’s life. This tool has been shown to be reliable and valid for assessing disability in children and adolescents and was found to be easy to complete and use within an active clinical setting. It can provide the impact of migraines on a child’s day-to-day activity and overall quality of life. The instrument also provides a useful tool to assess treatment outcomes and compare responses to individual therapies .
In order to compare the biochemical, anthropometric characteristics of both populations a t-Test and the Chi-square test, when appropriate, were performed.
To evaluate the differences in the sleep items pathological score of the SDSC in the original populations, a cut-off of at least 3 episodes per week was considered, according to the validation criteria . Therefore, the Chi-Square test was used to analyse the results.
In order to select from the original sample (MoA and normal), a representative group for PSG recordings the sample size was calculated with the on line software http://www.dssresearch.com/toolkit/sscalc/size_a2.asp with an Alpha Error Level at 5% and Beta Error Level at 50%.
In the group who underwent PSG study (34 MoA vs. 51 normal children), the comparisons between sleep architecture parameters were conducted using the nonparametric Mann–Whitney U test for independent data sets .
In order to evaluate the PLMd influence on headache characteristics, the MoA sample was divided in two groups accordingly the periodic limb movement index (PLMI) ≥5/h . Then, the t-Test and, when appropriate, the Chi-square test were performed to compare MoA characteristics (i.e. frequency, intensity, duration of attacks, life impairment and treatment efficacy) of two subgroups (MoA children with PLMI > 5/h and children with MoA with PLMI < 5/h).
In order to analyze the relationship among PLMI with frequency, duration, intensity and disability of MoA children, the Pearson’s correlation test was computed.
For all statistical analysis, p values <0.05 were considered significant.
Sleep habits in migraine without aura and control children
MoA (n = 187) (%)
Control (n = 766) (%)
1. Sleep less than 8 h
2. Sleep latency >30 min
3. Reluctant to go to bed
4. Difficulty getting to sleep at night
5. Anxiety when falling asleep
6. Hypnic jerks
7. Rhythmic movements while falling asleep
8. Vivid dream-like scenes while falling asleep
9. Falling asleep sweating
10. More than two awkenings per night
11. Difficulty to fall asleep after awakenings
12. Nocturnal hyperkinesias
13. Sleep breathing difficulties
14. Sleep apnea
16. Night sweating
18. Sleep talking
19. Teeth grinding
20. Sleep terrors
22. Difficulty in waking up in the morning
23. Feeling tired awakening in the morning
24. Sleep paralysis
25. Daytime somnolence
26. Sleep attacks
According to the sample size calculation, the size of both groups who underwent PSG (34 migraine and 51 normal children) was representative of starting population.
Demographic, anthropometric and biochemical evaluation in MoA and normal comparisons, who underwent the polysomnographic study
MoA (n = 34)
Control (n = 51)
10.67 ± 2.6
10.92 ± 2.37
Sex ratio (M/F)
z-BMI (z score Body Mass Index)
0.31 ± 0.43
0.21 ± 0.37
13.04 ± 0.97
13.1 ± 1.05
Serum iron, (μg/dL)
80.30 ± 17.21
79.95 ± 18.04
Serum ferritin, (μg/L)
34.5 ± 16.2
31.97 ± 15.1
Transferrin saturation (%)
23.51 ± 5.14
22.76 ± 6.32
Sleep macrostructural, respiratory parameters and PLM nocturnal evaluation
Migraine (N = 34)
Control (N = 51)
There were not differences in sleep stage percentages and in respiratory indexes, such as apnea/hypopnea index (AHI) and oxygen desaturation index (ODI) between the two groups.
Comparison about pain characteristics, disability and treatment efficacy between MoA children with p values <0.05 was considered significant
PLMI > 5/h (9)
PLMI < 5/h (25)
15.667 ± 2.236
6.840 ± 2.838
8.444 ± 1.014
5.200 ± 1.848
8.778 ± 2.108
5.320 ± 3.262
63.556 ± 5.27
24.88 ± 10.41
Preventive therapy efficacy
Moreover, the Pearson’s analysis shows a positive correlation between PLMI and frequency (r = .5925; p < 0.001), intensity (r = .4922; p = 0.003), duration (r = .3968; p = 0.02) and disability due to migraine (r = .6931; p < 0.001).
The main findings of our study can be summarised in the assessing of PLMd prevalence in children affected by MoA, and in the identification as potential causative role of PLMd in disability and pain intensity in children affected by migraine without aura.
In general, the inter-relationship between sleep and headache seems to interest also the sleep length: an excess or lack of sleep or a bad quality or inadequate duration of sleep could cause headache [2, 4].
In fact, the short sleepers tend to exhibit significantly more frequent headaches than long sleepers and were also more likely to experience morning headaches at awakening .
Moreover, previous studies described the differences in sleep habits such as a higher quote of DIMS, SBD, DA, SWTD and DES categories , and in the sleep macrostructure such as a reduction in total sleep time (TST), rapid eye movement (REM) and slow-wave sleep (SWS), and an increased sleep latency (SOL)  between headache children respect of normal children, as confirmed by our findings.
In particular, our findings tend to confirm the reported differences respect of typical developing comparisons such as a higher sleep latency, higher rate in difficulty getting to sleep at night, anxiety when falling asleep, hypnic jerks, NREM parasomnias signs and sleep related movement disorders in SDSC subitems than control group. Moreover, accordingly with Vendrame study results , our MoA children present a reduction in TIB (p < 0.001), SPT (p < 0.001), and TST (p < 0.001) with a higher quote of awakenings per hour (p = 0.008) and PLM index (p < 0.001) than controls.
Alternatively, the PLMd have been reported with a variable prevalence in developmental age, after the first description by Pichietti and Walters . Genetic factors, altered iron metabolism and dopaminergic dysfunction have been thought to be involved in the pathophysiology of PLMd.
Accordingly, in our sample all these disturbances and alterations in iron metabolism were excluded.
Moreover, the present study, first tried to assess the prevalence of PLMd according to the PSG diagnosis in children with migraine that represents the 26.47% of our migraine sample.
Anyway, the lack of normative controls for prevalence of “any PLMS” in the general population is also limiting, as we cannot confidently infer how the prevalence of “any PLMS” in children with migraine compares to the prevalence in the general pediatric population.
On the other hand, migraine may be considered a painful disabling condition, particularly in childhood, and is often accompanied by severe impairments, including low quality emotional functioning, absenteeism from school, and poor academic performance, as well as poor cognitive functioning [40, 41], motor coordination,  sleep habits [37, 38, 43–49] and high maternal stress [50, 51].
Otherwise, there is no consensus about the MoA origin, pathophysiology and long-term course, particularly in the pediatric population , even if also several brain neurotransmitter systems have been suggested to be involved in migraine, such as glutamate, noradrenaline and for neuromodulators and dopamine .
In this light, our data seem to suggest that PLMd could influence the migraine clinical presentation, increasing its severity, frequency and all disabling aspects, such as the treatment efficacy also.
On the other hand, a recent report pinpointed a correlation between the pain threshold in adults affected by migraine and the sleep pressure, suggesting that migraineurs on the average tend to suffer from a relative sleep deprivation and need more sleep than healthy controls .
We should take into account the main limitation of this study represented by the fact that our subjects came from a small group from a specific region of Southern Italy.
Notwithstanding these limitations, this could be considered the first report about the potential value of the determination of the PLMd signs, and the importance of the PSG evaluation in children affected by migraine, particularly when the clinical and pharmacological management tend to fail in the attacks control.
- Paiva T, Farinha A, Martins A, Batista A, Guilleminault C: Chronic headaches and sleep disorders. Arch Intern Med 1997, 157: 1701–1705. 10.1001/archinte.1997.00440360117014PubMedView ArticleGoogle Scholar
- Jennum P, Jensen R: Sleep and headache. Sleep Med Rev 2002, 6: 471–479. 10.1053/smrv.2001.0223PubMedView ArticleGoogle Scholar
- Montagna P: Hypothalamus, sleep and headaches. Neurol Sci 2006, 27: S138-S143. 10.1007/s10072-006-0589-8PubMedView ArticleGoogle Scholar
- Sahota PK, Dexter JD: Sleep and headache syndromes: a clinical review. Headache 1990,30(2):80–84. 10.1111/j.1526-4610.1990.hed3002080.xPubMedView ArticleGoogle Scholar
- Allen RP, Picchietti D, Hening WA, Trenkwalder C, Walters AS, Montplaisi J: Restless Legs Syndrome Diagnosis and Epidemiology workshop at the National Institutes of Health; International Restless Legs Syndrome Study Group. 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(2):101–119. 10.1016/S1389-9457(03)00010-8PubMedView ArticleGoogle Scholar
- Nichols DA, Allen RP, Grauke JH, Brown JB, Rice ML, Hyde PR, Dement WC, Kushida CA: Restless legs syndrome symptoms in primary care: a prevalence study. Arch Intern Med 2003,63(19):2323–2329.View ArticleGoogle Scholar
- American Academy of Sleep Medicine: International Classification of Sleep Disorders. 2nd edition. Westchester, Illinois: Diagnostic and Coding Manual. American Academy of Sleep Medicine; 2005.Google Scholar
- Atlas Task Force: Recording and scoring leg movements. Sleep 1993, 16: 748–759.Google Scholar
- Zucconi M, Ferri R, Allen R, Baier PC, Bruni O, Chokroverty S, Ferini-Strambi L, Fulda S, Garcia-Borreguero D, Hening WA, Hirshkowitz M, Högl B, Hornyak M, King M, Montagna P, Parrino L, Plazzi G, Terzano MG: International Restless Legs Syndrome Study Group (IRLSSG). The official World Association of Sleep Medicine (WASM) standards for recording and scoring periodic leg movements in sleep (PLMS) and wakefulness (PLMW) developed in collaboration with a task force from the International Restless Legs Syndrome Study Group (IRLSSG). Sleep Med 2006,7(2):175–183. 10.1016/j.sleep.2006.01.001PubMedView ArticleGoogle Scholar
- Iber C, Ancoli-Israel S, Chesson AL, Quan SF: The AASM manual for the scoring of sleep and associated events: rules, terminology, and technical specifications. 1st edition. Westchester, IL: American Academy of Sleep Medicine; 2007.Google Scholar
- Lesage S, Hening WA: The restless legs syndrome and periodic limb movement disorder: a review of management. Semin Neurol 2004,24(3):249–259. 10.1055/s-2004-835066PubMedView ArticleGoogle Scholar
- O’Brien LM, Ivanenko A, Crabtree VM, Holbrook CR, Bruner JL, Klaus CJ, Gozal D: Sleep disturbances in children with attention deficit hyperactivity disorder. Pediatr Res 2003,54(2):237–243. 10.1203/01.PDR.0000072333.11711.9APubMedView ArticleGoogle Scholar
- 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(6):735–738.PubMedGoogle Scholar
- Khatwa U, Kothare SV: Restless legs syndrome and periodic limb movements disorder in the pediatric population. Curr Opin Pulm Med 2010,16(6):559–567. 10.1097/MCP.0b013e32833f11aePubMedView ArticleGoogle Scholar
- Kirk VG, Bohn S: Periodic limb movements in children: prevalence in a referred population. Sleep 2004, 27: 313–315.PubMedGoogle Scholar
- 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: 57–61.PubMed CentralPubMedGoogle Scholar
- Chervin RD, Hedger KM: Clinical prediction of periodic leg movements during sleep in children. Sleep Med 2001, 2: 501–510. 10.1016/S1389-9457(01)00069-7PubMedView ArticleGoogle Scholar
- Headache Classification Subcommittee of the International Headache Society: The International Classification of Headache Disorders, ed. 2. Cephalalgia 2004,24(Suppl. 1):1–15.Google Scholar
- World Medical Association: World Medical Association Declaration of Helsinki: Ethical Principles for Medical Research Involving Human Subjects. 2008. Available at: (retrieved 06 December 2012) http://www.wma.net/en/30publications/10policies/b3/ Google Scholar
- Looker AC, Dallman PR, Carroll MD, Gunter EW, Johnson CL: Prevalence of iron deficiency in the United States. JAMA 1997, 277: 973–976. 10.1001/jama.1997.03540360041028PubMedView ArticleGoogle Scholar
- Cole TJ: The LMS method for constructing normalized growth standards. Eur J Clin Nutr 1990, 44: 45–60.PubMedGoogle Scholar
- Bruni O, Ottaviano S, Guidetti V, Romoli M, Innocenzi M, Cortesi F, Giannotti F: The Sleep Disturbance Scale for Children (SDSC). Construction and validation of an instrument to evaluate sleep disturbances in childhood and adolescence. J Sleep Res. 1996,5(4):251–261. 10.1111/j.1365-2869.1996.00251.xPubMedView ArticleGoogle Scholar
- Eitner S, Urschitz MS, Guenther A, Urschitz-Duprat PM, Bohnhorst B, Schlaud M, Poets CF: Sleep problems and daytime somnolence in a German population-based sample of snoring school-aged children. J Sleep Res 2007, 16: 96–101. 10.1111/j.1365-2869.2007.00560.xPubMedView ArticleGoogle Scholar
- Spruyt K, Cluydts R, Verleye GB: Pediatric sleep disorders: exploratory modulation of their relationships. Sleep 2004, 27: 495–501.PubMedGoogle Scholar
- Esposito M, Carotenuto M: Borderline intellectual functioning and sleep: the role of cyclic alternating pattern. Neurosci Lett 2010, 485: 89–93. 10.1016/j.neulet.2010.08.062PubMedView ArticleGoogle Scholar
- Carotenuto M, Esposito M, D’Aniello A, Rippa CD, Precenzano F, Pascotto A, Bravaccio C, Elia M: Polysomnographic findings in Rett syndrome: a case–control study. Sleep Breath 2013,17(1):93–98. 10.1007/s11325-012-0654-xPubMedView ArticleGoogle Scholar
- Esposito M, Carotenuto M: Intellectual disabilities and power spectra analysis during sleep: a new perspective on borderline intellectual functioning. J Intellect Disabil Res 2013. in press 10.1111/jir.12036Google Scholar
- Carotenuto M, Gallai B, Parisi L, Roccella M, Esposito M: Acupressure therapy for insomnia in adolescents: a polysomnographic study. Neuropsychiatr Dis Treat. 2013, 9: 157–162.PubMed CentralPubMedGoogle Scholar
- Jasper HH: The 10–20 electrode system of the International Federation. Electroencephalogr Clin Neurophysiol 1958, 10: 370–375.View ArticleGoogle Scholar
- Rechtschaffen A, Kales A: A Manual of Standardized Terminology, Techniques, and Scoring System for Sleep Stages of Human Subjects. Washington, DC: Public Health Service, US Government Printing Office; 1968.Google Scholar
- American Thoracic Society: Standards and indications for cardiopulmonary sleep studies in children. Am J Respir Crit Care Med 1996, 153: 866–878.View ArticleGoogle Scholar
- Marcus CL, Omlin KJ, Basinki DJ, Bailey SL, Rachal AB, Von Pechmann WS, Keens TG, Ward SL: Normal polysomnographic values for children and adolescents. Am Rev Respir Dis 1992,146(5 Pt 1):1235–1239.PubMedView ArticleGoogle Scholar
- Traeger N, Schultz 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. 10.1002/ppul.20236PubMedView ArticleGoogle Scholar
- Hershey AD, Powers SW, Vockell AL, LeCates S, Kabbouche MA, Maynard MK: PedMIDAS: development of a questionnaire to assess disability of migraines in children. Neurology 2001,11;57(11):2034–2039.View ArticleGoogle Scholar
- Conover WJ: Practical nonparametric statistics. 3rd edition. New York: John Wiley & Sons; 1999.Google Scholar
- Kelman L, Rains JC: Headache and sleep: examination of sleep patterns and complaint in a large clinical sample of migraineurs. Headache 2005, 45: 904–910. 10.1111/j.1526-4610.2005.05159.xPubMedView ArticleGoogle Scholar
- Carotenuto M, Guidetti V, Ruju F, Galli F, Tagliente FR, Pascotto A: Headache disorders as risk factors for sleep disturbances in school aged children. J Headache Pain 2005,6(4):268–270. 10.1007/s10194-005-0204-zPubMed CentralPubMedView ArticleGoogle Scholar
- Vendrame M, Kaleyias J, Valencia I, Legido A, Kothare SV: Polysomnographic findings in children with headaches. Pediatr Neurol 2008,39(1):6–11. 10.1016/j.pediatrneurol.2008.03.007PubMedView ArticleGoogle Scholar
- Picchietti DL, Walters AS: Moderate to severe periodic limb movement disorder in childhood and adolescence. Sleep 1999, 22: 297–300.PubMedGoogle Scholar
- Kernick D, Campbell J: Measuring the impact of headache in children: a critical review of the literature. Cephalalgia 2009, 29: 3–16. 10.1111/j.1468-2982.2008.01693.xPubMedView ArticleGoogle Scholar
- Esposito M, Pascotto A, Gallai B, Parisi L, Roccella M, Marotta R, Lavano SM, Gritti A, Mazzotta G, Carotenuto M: Can headache impair intellectual abilities in children? An observational study. Neuropsychiatr Dis Treat. 2012, 8: 509–513.PubMed CentralPubMedView ArticleGoogle Scholar
- Esposito M, Verrotti A, Gimigliano F, Ruberto M, Agostinelli S, Scuccimarra G, Pascotto A, Carotenuto M: Motor coordination impairment and migraine in children: a new comorbidity? Eur J Pediatr 2012,171(11):1599–1604. 10.1007/s00431-012-1759-8PubMedView ArticleGoogle Scholar
- Carotenuto M, Esposito M, Precenzano F, Castaldo L, Roccella M: Cosleeping in childhood migraine. Minerva Pediatr 2011, 63: 105–109.PubMedGoogle Scholar
- Carotenuto M, Esposito M, Pascotto A: Migraine and enuresis in children: an unusual correlation? Med Hypotheses 2010, 75: 120–122. 10.1016/j.mehy.2010.02.004PubMedView ArticleGoogle Scholar
- Esposito M, Roccella M, Parisi L, Gallai B, Carotenuto M: Hypersomnia in children affected by migraine without aura: a questionnaire-based case–control study. Neuropsychiatr Dis Treat 2013, 9: 289–294.PubMed CentralPubMedGoogle Scholar
- Esposito M, Gallai B, Parisi L, Roccella M, Marotta R, Lavano SM, Mazzotta G, Carotenuto M: Primary nocturnal enuresis as a risk factor for sleep disorders: an observational questionnaire-based multicenter study. Neuropsychiatric Disease and Treatment 2013, 9: 437–443.PubMed CentralPubMedGoogle Scholar
- Bruni O, Novelli L, Guidetti V, Ferri R: Sleep and headaches during adolescence. Adolesc Med State Art Rev 2010,21(3):446–456. viiiPubMedGoogle Scholar
- Bruni O, Russo PM, Ferri R, Novelli L, Galli F, Guidetti V: Relationships between headache and sleep in a non-clinical population of children and adolescents. Sleep Med 2008,9(5):542–548. 10.1016/j.sleep.2007.08.010PubMedView ArticleGoogle Scholar
- Bruni O, Galli F, Guidetti V: Sleep hygiene and migraine in children and adolescents. Cephalalgia 1999,19(25):57–59.PubMedGoogle Scholar
- De Bruyne E, Van Hoecke E, Van Gompel K, Verbeken S, Baeyens D, Hoebeke P, Vande Walle J: Problem behavior, parental stress and enuresis. J Urol 2009,182(4 Suppl):2015–2020.PubMedView ArticleGoogle Scholar
- Esposito M, Gallai B, Parisi L, Roccella M, Marotta R, Lavano SM, Gritti A, Mazzotta G, Carotenuto M: Maternal stress and childhood migraine: a new perspective on management. Neuropsychiatr Dis Treat. 2013, 9: 351–355.PubMed CentralPubMedView ArticleGoogle Scholar
- Balottin U, Chiappedi M, Rossi M, Termine C, Nappi G: Childhood and adolescent migraine: a neuropsychiatric disorder? Med Hypotheses 2011,76(6):778–781. 10.1016/j.mehy.2011.02.016PubMedView ArticleGoogle Scholar
- D’Andrea G, Leon A: Pathogenesis of migraine: from neurotransmitters to neuromodulators and beyond. Neurol Sci 2010,31(Suppl 1):S1-S7.PubMedView ArticleGoogle Scholar
- Engstrøm M, Hagen K, Bjørk MH, Stovner LJ, Gravdahl GB, Stjern M, Sand T: Sleep quality, arousal and pain thresholds in migraineurs: a blinded controlled polysomnographic study. J Headache Pain 2013,14;14(1):12.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.