Literature DB >> 33074178

Gross Motor Function Disorders in Patients with Alternating Hemiplegia of Childhood.

Agnieszka Stępień1, Katarzyna Maślanko2, Maciej Krawczyk1, Witold Rekowski3, Anna Kostera-Pruszczyk4.   

Abstract

BACKGROUND: Alternating hemiplegia of Childhood (AHC) is a rare disease manifested by transient episodes of hemiplegia and other neurological disorders. Delayed motor development has been reported in patients with AHC, but detailed features of the motor impairment have not been described so far. AIM: The aim of the study was to evaluate gross motor function between attacks in a group of Polish patients with AHC.
MATERIALS AND METHODS: The interictal gross motor function was assessed using the Gross Motor Function AHC scale, which consisted of 41 motor tasks. The study group consisted of 10 patients with AHC older than 2 years of age. The control group consisted of 30 age- and gender-matched subjects. The results achieved in each of the 41 tasks by the study subjects were compared to the results obtained with controls using the non-parametric Mann-Whitney U-test. In tasks 38-41, mean times were compared between the study subjects and controls.
RESULTS: The study revealed gross motor function impairment in patients with AHC. The greatest differences compared to controls concerned such skills as standing on toes, walking on toes, walking on heels, as well as running and hopping on one leg and on alternate legs. Significant impairment of the motor function of the upper limbs was also found.
CONCLUSIONS: The study confirmed motor function impairment between attacks in patients with AHC. The study findings may indicate the need to introduce individualised physiotherapy management of patients with AHC.

Entities:  

Keywords:  alternating hemiplegia of childhood; child development; gross motor function disorders; physiotherapy; rare diseases

Mesh:

Year:  2020        PMID: 33074178      PMCID: PMC8518102          DOI: 10.34763/jmotherandchild.2020241.1935.000003

Source DB:  PubMed          Journal:  J Mother Child        ISSN: 1428-345X


Introduction

Alternating hemiplegia of childhood (AHC) is a rare neurological disease characterised by recurrent hemiplegic attacks and other paroxysmal symptoms, abolished with sleep. The incidence is estimated at 1 per 1,000,000 births (1). AHC was first described by Verret and Steele in 1971 (2). Most cases of AHC are attributed to de novo mutations in the ATP1A3 gene coding for alpha-3 catalytic subunit of the Na+/K(+)-ATPase (3,4,5). Paroxysmal symptoms include episodes of hemiplegia, bilateral hemiplegia, quadriplegia, dystonia, tonic spells, seizures and abnormal eye movements (5,6,7,8). Also observed are respiratory difficulty, dysarthria, dysphagia, facial dyskinesia or athetosis, as well as autonomic disturbances such as bradycardia, stridor, bronchospasm, changes in skin color, excessive constriction or dilation of the pupils, vomiting, diarrhoea, sweating, hyperthermia, hypothermia or excessive salivation (5,6,7,8,9,10,11). The hemiplegic episodes vary in frequency and duration (6). The clinical status of AHC sufferers varies during and between attacks (5). Intellectual and motor development is impaired in most patients with AHC (10,12). Tone abnormalities, choreoathetosis, ataxia and motor clumsiness are observed (8). Fine motor skills, cognitive development and behaviour are also affected (5).

Aim of the Study

The aim of the study was to assess gross motor function between attacks in a group of Polish patients with diagnosed AHC and to describe the disease-specific motor deficits between attacks. The results of the study may allow the design of a dedicated physiotherapy programme for patients with AHC.

Materials and Methods

The study was conducted from November 2014 until the end of May 2015. Contact with the patients was facilitated by the Polish Association for Persons with AHC (AHC-PL), which is a nongovernmental, not-for-profit and support organisation promoting the interests of and acting on behalf of patients with AHC. The subjects were included in the study when AHC was diagnosed by a neurologist or geneticist based on the Aicardi criteria (13). To qualify for a detailed assessment of gross motor capabilities, the subject had to be >2 years of age. The exclusion criteria included a hemiplegic attack during the study or feeling unwell, which made administration of the tests impossible. A control group was established for comparison with gross motor function assessments in AHC patients. For each study subject, three age (+ 6 months)- and gender-matched controls were randomly selected, i.e. a total of 30 controls. The exclusion criteria for controls included the following: participation in competitive sports; post-injury status or surgical operation within the past 12 months; or feeling unwell, which made completing the study impossible. The parents of the children and the adults participating in the study were informed about its aims, and they signed the consent to participate in the study and publish data form. The study was approved by the Senate Research Ethics Committee at the Józef Piłsudski University of Physical Education in Warsaw, Poland (SKE 01–07/2015). Fourteen patients with AHC, aged 1.2–30.1 years, and/or their carers expressed their wish to participate in the study. All of the subjects were members of the Polish Association for persons with AHC (AHC-PL). Two children below 2 years of age were not included in the detailed assessment of gross motor function because of their young age, and two patients were excluded from the study due to an ongoing hemiplegic attack. Ultimately, the study was completed by 10 subjects (four females and six males) >2 years of age. Mutations of ATP1A3 were identified in seven subjects. The information on age, height and weight of the study patients, as well as that of the age- and gender-matched controls, is presented in . Characteristics of the study (AHC) and control groups The study consisted of two parts. The subjects with diagnosed AHC and/or their carers first completed a questionnaire providing personal details and history of the disease, and next, the gross motor function was assessed. AHC patients and/or their carers reported typical signs, such as plegic attacks, tonic/dystonic attacks, nystagmus, deviation of the eyes, episodic respiratory difficulties and episodic autonomic disturbances. The plegic attacks occurred from a few to 20–30 times a month and lasted from a few minutes to several days. A detailed list of signs and symptoms, frequency and duration of the attacks in individual study subjects is presented in . Characteristics of the study (AHC) group – signs Gross motor function was assessed using the Gross Motor Function AHC (GMF AHC) scale proposed by the authors, comprising 41 motor tasks ranked by order of appearance of motor skills in human motor development (). The GMF AHC scale was based on various published motor function scales, mainly on the Hammersmith Functional Motor Scale – Expanded (HFMSE) and the Gross Motor Function Measure (GMFM), and it included other motor tasks proposed by the authors of the study and which were selected after appropriate pilot studies. The GMF AHC scale used 23 items from the HFMSE and 2 items from the GMFM. Because of the differences in age and motor function status among the patients, after an initial assessment of some of them, 16 new motor tasks were added. The HFMS was originally developed to assess function in non-ambulant children with spinal muscular atrophy. The scale was later modified, extended (HFMSE) and validated (14,15,16). Authors used the following sub-tests from HFMSE: 1. Lifts head from supine position; 2. Moves from lying to sitting position; 3. Duration of sitting; 4. Duration of long sitting; 5. Places right hand on head while sitting, hand touching the head above the level of ears; 6. Places left hand on head while sitting, hand touching the head above the level of ears; 7. Places two hands on head while sitting, hands touching the head above the level of ears; 8. Moves from sitting to lying position; 9. Moves from supine position to lying on side; 10. Rolls over from supine position to prone position on the right; 11. Rolls over from prone position to supine position on the right; 12. Rolls over from supine position to prone position on the left; 13. Rolls over from prone position to supine position on the left; 14. Lifts head from the prone position; 15. Props on forearms; 16. Props on extended arms; 17. Performs four-point kneeling; 18. Performs crawling; 20. Executes supported standing; 21. Stands unsupported; 22. Squats; 33. Ascends stairs without rail; 34. Descends stairs without rail. The GMFM was originally designed to assess gross motor function in children with cerebral palsy (17). It has also been used and validated in children with other diseases associated with significant motor impairment (18,19,20). The authors used the following sub-tests from GMFM: 24. Walks forward; 28. Runs. The new motor tasks added by the authors were as follows: 19. Gets to standing position from a supine position; 23. Gets off a chair without using arms; 25. Stands on toes; 26. Walks on toes; 27. Walks on heels; 29. Hops on both legs; 30. Hops on right foot; 31. Hops on left foot; 32. Hops on alternate legs; 35. Catches a ball with both hands, stands – ball 25 cm, five attempts; 36. Throws a tennis ball – dominant hand, stands, five attempts; 37. Kicks ball – dominant leg, stands, ball 20 cm, 3 m, five attempts; 38. Stands on right leg with eyes open, hands crossed on chest; 39. Stands on left leg with eyes open, hands crossed on chest; 40. Stands on right leg with eyes closed, hands crossed on chest; 41. Stands on left leg with eyes closed, hands crossed on chest. The validation of the GMF AHC prior to the study was impossible to perform due to the extremely small number of patients. The patients and controls were tested by four qualified physiotherapists. The tests were carried out on patients in the lying, sitting and standing positions. Tasks 1–37 could score 0, 1 or 2 points (0= task not performed; 1= task partially performed; 2= task normally performed), while in tasks 38–41, the time it took the subject to perform the task was measured. Tasks 38–41 had to be performed in triplicate up to 15 seconds in duration, and the best result was recorded. Instructions for each motor task were given to the subject verbally, followed by a demonstration by the investigator. The results for the study subjects were analysed using the SPSS software. The results achieved in each of the 41 tasks by the study subjects were compared to the results for controls using the non-parametric Mann–Whitney U-test. In tasks 38–41, the mean times were compared between the study subjects and controls. The results were considered statistically significant at p<0.05.

Results

Tests for gross motor function in subjects aged 2–30 years found statistically significant differences between the study group and controls in 22 tasks (Table 3). The study subjects achieved significantly worse results in the following sub-tests: 19. Gets to standing from a supine position; 21. Stands unsupported; 22. Squats; 23. Gets off a chair without using arms; 24. Walks forward; 25. Stands on toes; 26. Walks on toes; 27. Walks on heels; 28. Runs; 29. Hops on both legs; 30. Hops on right leg; 31. Hops on left leg; 32. Hops on alternate legs; 33. Ascends stairs without rail; 34. Descends stairs without rail; 35. Catches a ball with both hands; 36. Throws a tennis ball; 37. Kicks ball – dominant leg; 38. Stands on right leg with eyes open; 39. Stands on left leg with eyes open; 40. Stands on right leg with eyes closed; 41. Stands on left leg with eyes closed.
Table 3

Gross Motor Function AHC scale – differences between study (AHC) and control groups

Item Gross Motor Function AHC Study (AHC) group Gross Motor Function AHC Control group p

Mean ± SD SE Mean ± SD SE
1. Lifts head from supine position1.90 ± 0.320.101.93 ± 0.250.050.73
2. Lying to sitting position1.90 ± 0.320.102.00 ± 0.000.000.08
3. Sitting position2.00 ± 0.000.002.00 ± 0.000.001.00
4. Long sitting position2.00 ± 0.000.002.00 ± 0.000.001.00
5. Right hand to head in sitting position1.90 ± 0.320.102.00 ± 0.000.000.08
6. Left hand to head in sitting position1.90 ± 0.320.102.00 ± 0.000.000.08
7. Two hands to head in sitting position1.90 ± 0.320.102.00 ± 0.000.000.08
8. Sitting to lying position2.00 ± 0.000.002.00 ± 0.000.001.00
9. Supine position to lying on side2.00 ± 0.000.002.00 ± 0.000.001.00
10. Rolls from supine position to prone position over right1.90 ± 0.320.102.00 ± 0.000.000.08
11. Rolls from prone position to supine position over right1.90 ± 0.320.102.00 ± 0.000.000.08
12. Rolls from supine position to prone position over left1.90 ± 0.320.102.00 ± 0.000.000.08
13. Rolls from prone position to supine position over left1.90 ± 0.320.102.00 ± 0.000.000.08
14. Lifts head from prone position2.00 ± 0.000.002.00 ± 0.000.001.00
15. Props on forearms2.00 ± 0.000.002.00 ± 0.000.001.00
16. Props on extended arms2.00 ± 0.000.002.00 ± 0.000.001.00
17. Achieves four-point kneeling1.90 ± 0.320.102.00 ± 0.000.000.08
18. Crawls2.00 ± 0.000.002.00 ± 0.000.001.00
19. Gets to standing from a supine position1.60 ± 0.840.272.00 ± 0.000.000.01*
20. Executes supported standing1.80 ± 0.630.202.00 ± 0.000.000.08
21. Stands unsupported1.60 ± 0.840.272.00 ± 0.000.000.01*
22. Squats0.96 ± 0.610.191.79 ± 0.460.080.00*
23. Gets off a chair without using arms1.60 ± 0.840.272.00 ± 0.000.000.01*
24. Walks forward1.60 ± 0.840.272.00 ± 0.000.000.01*
25. Stands on toes0.50 ± 0.530.171.90 ± 0.310.060.00*
26. Walks on toes1.18 ± 0.900.282.00 ± 0.000.000.00*
27. Walks on heels0.70 ± 0.820.262.00 ± 0.000.000.00*
28. Runs0.94 ± 0.880.281.94 ± 0.130.020.00*
29. Hops on both legs1.30 ± 0.820.262.00 ± 0.000.000.00*
30. Hops on right foot0.40 ± 0.840.271.90 ± 0.310.060.00*
31. Hops on left foot0.40 ± 0.840.271.83 ± 0.380.070.00*
32. Hops on alternate legs0.43 ± 0.560.181.56 ± 0.480.090.00*
33. Ascends stairs without rail1.25 ± 0.780.251.92 ± 0.200.040.00*
34. Descends stairs without rail1.25 ± 0.780.251.92 ± 0.200.040.00*
35. Catches a ball with both hands1.20 ± 0.790.251.93 ± 0.250.050.00*
36. Throws a tennis ball1.60 ± 0.840.272.00 ± 0.000.000.01*
37. Kicks ball – dominant leg1.60 ± 0.840.272.00 ± 0.000.000.01*
38. Stands on right leg with eyes open3.58 ± 5.011.5911.92 ± 4.590.840.00*
39. Stands on left leg with eyes open3.78 ± 5.071.6011.81 ± 4.430.810.00*
40. Stands on right leg with eyes closed2.22 ± 3.521.118.82 ± 5.971.090.00*
41. Stands on left leg with eyes closed1.93 ± 2.480.799.03 ± 6.031.100.00*

SD, standard deviation; SE, standard error.

p calculated using the Mann–Whitney U–test;

p<0.05.

Gross Motor Function AHC scale – differences between study (AHC) and control groups SD, standard deviation; SE, standard error. p calculated using the Mann–Whitney U–test; p<0.05.

Discussion

Studies of AHC are relatively recent and, to date, cases of patients from a number of countries have been reported (10, 12, 21,22,23,24,25,26). The aim of the present study was to provide detailed characteristics of gross motor dysfunction in AHC patients. To the best of our knowledge, to date, no other such study has been performed. There are no available tools to assess gross motor function in AHC or to compare gross motor function in subjects who vary greatly in age. The motor tasks included in the Gross Motor Function AHC scale developed for the purpose of the present study allow the assessment of motor function in particular body parts and, as a result, a detailed description of the motor dysfunction in each subject. The Gross Motor Function AHC is based on items of the HFMSE and the GMFM, to which new sub-tests have been added. The advantage of the GMF AHC is its ability to assess the subject's performance in different positions, from lying prone and supine to standing, during both static and dynamic activities. However, the scoring system does not assess the quality and precision of the movements, which should be addressed in further studies. We found gross motor impairment in AHC subjects, in agreement with the reports from other authors, who observed delayed development in most individuals with AHC (5,10). In our study, AHC subjects achieved the worst results in the following tasks: standing and walking on toes, walking on heels, running, hopping on one leg and hopping on alternate legs. Walking abnormalities in AHC were also noted in other published studies (5). Kirshenbaum et al. (27) studied mice with mutations in the gene responsible for AHC. The animals had less-stable gait, walked with shorter steps and had poorer postural stability than wild-type mice (27). In the present study, two subjects aged 2.5 and 3.5 years were not able to walk independently. The results of the present study mostly indicate impaired control of the muscles producing plantar and dorsal flexion of the foot, stabilising muscles of the foot, as well as muscles straightening the knee and hip joints, which are active during hopping, walking and running. Additionally, the test results suggest impaired coordination and fluidity of movement, with a narrow base of support. Tests performed in a lying position did not reveal any dysfunction of trunk muscles. However, significantly impaired function of the upper limbs was observed during catching and throwing. Such a pattern of muscle function abnormalities is consistent with disturbances in consecutive phases of development and indicates generally delayed development. Interestingly, inability to perform alternate movements of the trunk and extremities was observed in all study patients. Our findings allow the development of AHC-specific physiotherapy management. They cannot be compared to other studies because, to our knowledge, there have been no published studies of this kind. It would be worthwhile to conduct similar studies involving a larger group of patients from different countries. Undoubtedly, the limitation of this research is the large discrepancy in age of the study subjects. Taking it into consideration, the authors randomly selected three age- and gender-matched controls for each AHC subject. This method of qualification was intended to reduce the effect of age on the results. The results of our research expand our knowledge about major motor disorders in AHC patients. It can be assumed that a dedicated physiotherapy management might improve the condition of AHC patients, but this requires confirmation in further studies.

Conclusion

Gross motor impairment is observed in patients with AHC between attacks. The present study mostly indicates impaired control of the muscles responsible for the functioning of the lower extremities. The study findings may indicate the need to introduce individualised physiotherapy management of patients with AHC, tailored to their motor development, but this requires further research.
Table 1

Characteristics of the study (AHC) and control groups

Study group (AHC) Control group

No. Gender Height (cm) Weight (kg) Age (years) Mutation of ATP1A3 No. Gender Mean height (cm) Mean weight (kg) Mean age (years)
1F8311.52.5+1.1; 1.2; 1.3F89.813.62.5
2M104143.5+2.1; 2.2; 2.3M100.3153.5
3M104193.53.1; 3.2; 3.3M103193.5
4F124236.2+4.1; 4.2; 4.3F121.3226.6
5F128229.15.1; 5.2. 5.3F141318.9
6M132269.1+6.1;6.2; 6.3M142.7379.2
7M1646012.87.1; 7.2;7.3M159.75312.9
8M1885020.3+8.1; 8.2; 8.3M1817420.5
9F1545224.3+9.1; 9.2; 9.3F16962.324.3
10M1847030.1+10.1;10.2;10.3M182.582.530.3
Table 2

Characteristics of the study (AHC) group – signs

No. Unilateral Attacks Bilateral attacks Signs Frequency (number of attacks per month) Average duration of episode Medicines
1++Plegic attacksTonic/dystonic attacksNystagmusDeviation of the eyesEpisodic respiratory difficultiesEpisodic autonomic disturbances1–230 min–2 hYes
2++Plegic attacksTonic/dystonic attacksNystagmusDeviation of the eyesEpisodic respiratory difficultiesEpisodic autonomic disturbances4–87 days–several daysNo
3++Plegic attacksTonic/dystonic attacksAtaxiaA fewA few minutes to few hoursYes
4++Plegic attacksTonic/dystonic attacksNystagmusDeviation of the eyes1–30A few minutes to 12 hNo
5+Tonic/dystonic attacksNystagmusEpisodic autonomic disturbances5–3030 s–1 minYes
6++Plegic attacksTonic/dystonic attacksDeviation of the eyesEpisodic respiratory difficulties10A few hours–2 daysYes
7++Plegic attacksTonic/dystonic attacksNystagmus1–20A few minutes to a few hoursYes
8++Plegic attacksTonic/dystonic attacksDeviation of the eyesEpisodic respiratory difficultiesEpisodic autonomic disturbancesOne to a fewA few hours to a few daysNo
9++Plegic attacksTonic/dystonic attacksNystagmusEpisodic respiratory difficultiesPlegic attacks17–20A few minutes to a few daysNo
10++Tonic/dystonic attacksDeviation of the eyesEpisodic respiratory difficultiesFew – 20Several minutes to a few hoursYes
Table S1

Gross Motor Function AHC

Item No. Item Points: 0 Points: 1 Points: 2
1Lifts head from supine positionUnableHead is lifted, but through side flexion or with no neck flexion. Held for a count of 3In supine position, head must be lifted in midline. Chin moves towards chest. Held for a count of 3
2Lying to sitting positionUnableTurns into prone position or towards floorAble to do by lying on side
3Sitting2 hands for support1 hand for support, for a count of 3No hand support, for a count of 3
4Long sitting 2 hands for support1 hand for support, for a count of 3No hand support, for a count of 3
5Right hand to head in sitting position Hand touches head above level of earsUnableCan only bring right hand to head by flexing headAble to bring right hand to head. Head and trunk remain stable
6Left hand to head in sitting position Hand touches head above level of earsUnableCan only bring left hand to head by flexing headAble to bring right hand to head. Head and trunk remain stable
7Two hands to head in sitting position Hands touch head above level of earsUnableAble to place hands on head but only using head flexion or side tiltAble to place both hands on head, arms free from side. Head and trunk remain stable
8Sitting to lying positionUnable or falls overAble to lie down by flopping forwards and rolling sidewaysAble to lie down in a controlled fashion through lying on side or using clothes
9Supine position to side-lying positionUnableCan ½ roll only one way: either right or leftAble to ½ roll from supine position both ways
10Rolls from supine position to prone position over right UnableTurns to prone position by pulling/pushing on armsTurns to prone position with free arms to the right
11Rolls from prone position to supine position over right UnableTurns to supine position using arms to push/pull withTurns to supine position with free arms to the right
12Rolls from supine position to prone position over leftUnableTurns to prone position by pulling/pushing on armsTurns to prone position with free arms to the left
13Rolls from prone position to supine position over leftUnableTurns to supine position using arms to push/pull withTurns to supine position with free arms to the left
14Lifts head from prone positionUnableLifts head with arms in a forward position for a count of 3Able to lift head up in prone position, arms by side for a count of 3
15Props on forearmsUnableHolds position when placed for a count of 3Able to achieve prop on elbows with head up for a count of 3
16Props on extended armsUnableHolds position when placedAchieves hands support in prone position
17Four-point kneeling UnableHolds position when placed for a count of 3Achieves four-point kneeling – head up for a count of 3
18CrawlingUnableMoves all four points only onceAble to crawl forwards – moves all four points twice or more
19Gets to standing position from a supine position§UnableUses furnitureAchieves standing without furniture
20Supported standingCan stand with hand support but needs knee/hip support in addition for a count of 3, unableAble to stand with minimal trunk support (not hip) for a count of 3Can stand using one hand support for a count of 3
21Stands unsupportedStands only momentarily, unableStands independently for a count of 3Can stand independently for more than a count of 3
22SquatsUnableInitiates squat (>10%), uses arm support, or static <3 secondsSquats with arms free (at least 90° of hip and knee flexion), static > 3 seconds
23Gets off a chair without using arms§UnableUses armsGets off independently without using arms
24Walks forwardUnableWalks <10 stepsWalks >10 steps
25Stands on toes§UnableStands <5 secondsStands >5 seconds
26Walks on toes§UnableWalks with assistance, <3 mWalks independently, >3 m
27Walks on heels§UnableWalks with assistance, <3 mWalks independently, >3 m
28RunsUnableRuns <4.5 mRuns >4.5 m, stops and returns
29Hops on both legs§Unable<5 consecutive hops>5 consecutive hops
30Hops on right foot§Unable<5 consecutive hops>5 consecutive hops
31Hops on left foot§Unable<5 consecutive hops>5 consecutive hops
32Hops on alternate legs§UnableDoes not hop on alternate legs and arms, <10 consecutive hopsHops on alternate legs and arms, >10 consecutive hops
33Ascends stairs without railUnableAscends <4 stairs, arms free, any pattern or with arm supportAscends 4 stairs, arms free, alternating feet
34Descends stairs without railUnableDescends <4 stairs, arms free, any pattern or with arm supportDescends 4 stairs, arms free, alternating feet
35Catches a ball with both hands, stands, ball 25 cm, 5 attempts§UnableCatches a ball with both hands, throws to a distance >1.5 mCatches a ball with both hands >4 times
36Throws a tennis ball, stands, dominant hand, 5 attempts§UnableThrows distance <1.5 m or throws to a distance >1.5 m < 4 timesThrows to a distance > 1.5 m, 4 or 5 times
37Kicks ball – dominant leg, stands, ball 20 cm, 3 m, 5 attempts §UnableKicks 3 m< 4 timesKicks 3 m> 4 times
38Stands on right leg with eyes open, hands crossed on chest §Timer
39Stands on left leg with eyes open, hands crossed on chest §Timer
40Stands on right leg with eyes closed, hands crossed on chest §Timer
41Stands on left leg with eyes closed, hands crossed on chest §Timer

Tasks based on the Hammersmith Functional Motor Scale Expanded (HFMSE);

the Gross Motor Function Measure (GMFM) and

other motor tasks.

  27 in total

1.  The gross motor function measure is a valid and sensitive outcome measure for spinal muscular atrophy.

Authors:  Leslie Nelson; Hollis Owens; Linda S Hynan; Susan T Iannaccone
Journal:  Neuromuscul Disord       Date:  2006-05-02       Impact factor: 4.296

2.  Validation of the Expanded Hammersmith Functional Motor Scale in spinal muscular atrophy type II and III.

Authors:  Allan M Glanzman; Jessica M O'Hagen; Michael P McDermott; William B Martens; Jean Flickinger; Susan Riley; Janet Quigley; Jacqueline Montes; Sally Dunaway; Liyong Deng; Wendy K Chung; Rabi Tawil; Basil T Darras; Darryl C De Vivo; Petra Kaufmann; Richard S Finkel
Journal:  J Child Neurol       Date:  2011-09-21       Impact factor: 1.987

3.  Evidence of a non-progressive course of alternating hemiplegia of childhood: study of a large cohort of children and adults.

Authors:  Eleni Panagiotakaki; Giuseppe Gobbi; Brian Neville; Friedrich Ebinger; Jaume Campistol; Sona Nevsímalová; Laura Laan; Paul Casaer; Georg Spiel; Melania Giannotta; Carmen Fons; Miriam Ninan; Guenter Sange; Tsveta Schyns; Rosaria Vavassori; Dominique Poncelin; Alexis Arzimanoglou
Journal:  Brain       Date:  2010-10-24       Impact factor: 13.501

4.  Using the gross motor function measure to evaluate motor development in children with Down syndrome.

Authors:  M Gémus; R Palisano; D Russell; P Rosenbaum; S D Walter; B Galuppi; M Lane
Journal:  Phys Occup Ther Pediatr       Date:  2001       Impact factor: 2.360

5.  Alternating hemiplegia of childhood in chinese following long-term treatment with flunarizine or topiramate.

Authors:  Ling-yi Chi; Xiu-he Zhao; Xue-wu Liu; Wen-jing Jiang; Zhao-fu Chi; Sheng-jun Wang
Journal:  Int J Neurosci       Date:  2012-05-11       Impact factor: 2.292

6.  Alternating hemiplegia of childhood in Denmark: clinical manifestations and ATP1A3 mutation status.

Authors:  Christina E Hoei-Hansen; Christine Í Dali; Troels J B Lyngbye; Morten Duno; Peter Uldall
Journal:  Eur J Paediatr Neurol       Date:  2013-09-25       Impact factor: 3.140

Review 7.  Distinct neurological disorders with ATP1A3 mutations.

Authors:  Erin L Heinzen; Alexis Arzimanoglou; Allison Brashear; Steven J Clapcote; Fiorella Gurrieri; David B Goldstein; Sigurður H Jóhannesson; Mohamad A Mikati; Brian Neville; Sophie Nicole; Laurie J Ozelius; Hanne Poulsen; Tsveta Schyns; Kathleen J Sweadner; Arn van den Maagdenberg; Bente Vilsen
Journal:  Lancet Neurol       Date:  2014-05       Impact factor: 44.182

8.  Alternating hemiplegia of childhood: early characteristics and evolution of a neurodevelopmental syndrome.

Authors:  Matthew T Sweney; Kenneth Silver; Marion Gerard-Blanluet; Jean-Michel Pedespan; Francis Renault; Alexis Arzimanoglou; Mylynda Schlesinger-Massart; Aga J Lewelt; Sandra P Reyna; Kathryn J Swoboda
Journal:  Pediatrics       Date:  2009-03       Impact factor: 7.124

9.  Heterozygous de-novo mutations in ATP1A3 in patients with alternating hemiplegia of childhood: a whole-exome sequencing gene-identification study.

Authors:  Hendrik Rosewich; Holger Thiele; Andreas Ohlenbusch; Ulrike Maschke; Janine Altmüller; Peter Frommolt; Birgit Zirn; Friedrich Ebinger; Hartmut Siemes; Peter Nürnberg; Knut Brockmann; Jutta Gärtner
Journal:  Lancet Neurol       Date:  2012-07-30       Impact factor: 44.182

10.  De novo mutations in ATP1A3 cause alternating hemiplegia of childhood.

Authors:  Erin L Heinzen; Kathryn J Swoboda; Yuki Hitomi; Fiorella Gurrieri; Sophie Nicole; Boukje de Vries; F Danilo Tiziano; Bertrand Fontaine; Nicole M Walley; Sinéad Heavin; Eleni Panagiotakaki; Stefania Fiori; Emanuela Abiusi; Lorena Di Pietro; Matthew T Sweney; Tara M Newcomb; Louis Viollet; Chad Huff; Lynn B Jorde; Sandra P Reyna; Kelley J Murphy; Kevin V Shianna; Curtis E Gumbs; Latasha Little; Kenneth Silver; Louis J Ptáček; Joost Haan; Michel D Ferrari; Ann M Bye; Geoffrey K Herkes; Charlotte M Whitelaw; David Webb; Bryan J Lynch; Peter Uldall; Mary D King; Ingrid E Scheffer; Giovanni Neri; Alexis Arzimanoglou; Arn M J M van den Maagdenberg; Sanjay M Sisodiya; Mohamad A Mikati; David B Goldstein
Journal:  Nat Genet       Date:  2012-07-29       Impact factor: 38.330

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  1 in total

1.  Different phenotypes of neurological diseases, including alternating hemiplegia of childhood and rapid-onset dystonia-parkinsonism, caused by de novo ATP1A3 mutation in a family.

Authors:  Wen Wei; Xiu-Fen Zheng; Dan-Dan Ruan; Yu-Mian Gan; Yan-Ping Zhang; Ying Chen; Xin-Fu Lin; Fa-Qiang Tang; Jie-Wei Luo; Yun-Fei Li
Journal:  Neurol Sci       Date:  2021-11-16       Impact factor: 3.307

  1 in total

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