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Abstract

PURPOSE:

To assess hand dexterity in children with myelomeningocele (MMC) and to explore factors related to hand dexterity in these children.

METHODS:

Ninety-four children with myelomeningocele, aged 4 to 18 years, were assessed. Demographic characteristics, disease factors, visual perception (Beery test of Visual Motor Integration), cognition (WeeFunctional Independence Measure), and self-care (Pediatric Evaluation of Disability Inventory) were assessed in relation to the Nine-Hole Peg Test (9HPT) for hand dexterity using Spearmen correlations and linear regressions.

RESULTS:

The children’s performance on the 9HPT in both hands was significantly slower than the norms for their age groups. Children without a shunt showed significantly better function in both hands (p = .005) than those with a shunt. Factors most related to hand dexterity were neurological spinal level of MMC, presence of shunt, age, cognitive ability, and years of mother’s education.

CONCLUSION:

Children with MMC appear to have poorer hand skills than typically developed children, which was related to pathology as well as functional and environmental factors. When addressing hand dexterity in children with MMC, it is important that rehabilitation professionals continue to work with these children as they get older, and put greater emphasis on parent education using materials that are adapted to varying educational levels.

Keywords

Myelomeningocele fine motor dexterity hydrocephalus cognition

1 Introduction

Myelomeningocele (MMC), a type of spina bifida, is a congenital disorder in which the neural tube does not close completely. MMC has an incidence worldwide of 4.7 in 10,000 live births [1] and results in a total or partial loss of sensation and motor paralysis distal to the level of the defect. Children with MMC often have Arnold Chiari malformation, a structural defect in the cerebellum and hindbrain [2]. Hydrocephalus, a buildup of cerebral spinal fluid in the brain resulting in increased pressure in the brain [3] occurs in about 95 percent of cases [4]. Children and adults with MMC generally have impairments in function including cognitive, ambulatory, bowel and bladder dysfunction, and difficulties performing self-care activities [5].

Although the spinal cord lesion is typically not in the cervical region, children with MMC often have impaired upper extremity function [6, 7]. They have weakness in the small muscles of their hands, and diminished fine motor dexterity and coordination than typically developing (TD) children in their age range [6]. They may also have difficulty with speed, inadequate precision grip force, impaired kinesthetic awareness of the hands and bilateral coordination [7].

Fine motor dexterity is an important skill for children, enabling them to perform daily living activities efficiently, and enhancing participation in various aspects of life [8]. The impaired fine motor function and diminished speed in performing tasks associated with MMC may come as a result of disruption of key structures such as the cerebellum with Arnold Chiari malformation and hydrocephalus in many of these children [9]. Upper limb weakness and spasticity in children with MMC may be a sign of brainstem compression and degeneration of the cerebellum [10]. There is some evidence that surgical decompression may lead to better clinical outcomes in the fine motor skills of patients with Chiari [11]. Indeed, children with a shunted hydrocephalus perform more poorly than those without a shunt [12, 13]. The organizational anatomy of the cortex in children with MMC is atypical including enlarged levels of cortical thickness and gyrification. These are associated with limited cognitive and fine motor outcomes [14], difficulties in visual motor integration and risk for learning disabilities [7]. While cognitive and executive functions are often associated with fine motor skills in TD children [15], some studies of those with MMC have not found a relationship between fine motor function and cognitive or academic function [7, 9]. In addition, while MMC with hydrocephalus has been found to be associated with difficulty with visual motor integration skills [16], the relationship between fine motor skills and visual perceptual skills in children with MMC has not been sufficiently investigated. Relationships between fine motor dexterity and postural control have been shown for typically developing children [17, 18]. Although this was not observed in a previous older study of MMC patients [19], higher levels of spinal pathology would be expected to affect both postural control and fine motor skills.

Environmental factors such as maternal age, parental education and socioeconomic status have also been found to be related to better fine motor skills in typically developing children [20]. However, the relationship between fine motor skills and environmental factors, severity of the condition and functional level does not appear to have been explored in children with MMC. Such interactions are important to identify since likely they will help health professionals adopt a more holistic approach when working on goal setting with these individuals. Impaired hand function has been found to be significantly related to dependence in daily living activities in children with MMC [21]. It is important to investigate in greater depth the factors that are related to hand skills in children with MMC since such difficulties can have an impact on their functional abilities and participation.

The objectives of this study were: 1. to evaluate hand dexterity in children with MMC in comparison to norms for their age range; 2. to investigate factors associated with hand dexterity in children with MMC and 3. to examine whether there is a relationship between hand dexterity and independence in self-care activities in children with MMC.

2 Methods

2.1 Participants

Ninety-four children with MMC (ages 4–18 years) were recruited from the multi-disciplinary spina bifida clinic at Alyn Hospital Pediatric and Adolescent Rehabilitation Center in Jerusalem, Israel over a period of one year. Out of the approximately 370 children and adolescents who visited the MMC clinic for annual follow-up visits, 100 met age range and eligibility criteria; parental consent to participate was received for 94 children. Children were excluded from the study if they had additional diagnoses which significantly impacted their function (e.g., Autism Spectrum Disorder), or had significant cognitive impairment preventing them from being able to communicate. The study protocol was approved by the hospital research ethics committee.

2.2 Instruments

A sociodemographic questionnaire included information regarding the educational setting, number of siblings, age of parents, level of parents’ education, and socioeconomic level.

The medical records of each child were scrutinized to note the neurological level as determined by the clinic pediatrician’s medical examination (including sensory and motor evaluation), associated hydrocephalus, number of shunts performed, and presence of Arnold Chiari malformation.

The Nine-Hole Peg Test (9HPT) (22), the primary outcome measure, is a reliable and valid tool for measuring fine motor dexterity in school aged children, with norms from ages 4 to 18 years [23]. The child is asked to place and then remove 9 wooden pegs into holes in a square pegboard. Time taken to complete the task is recorded, first with the dominant hand and then with the non-dominant hand. The results in seconds were transferred to Z scores, according to age and gender norms values [23] and referred to as the standard score of the 9HPT.

The Beery-Butenika Test of Visual Motor Integration [24] visual perceptual subtest is a widely used standardized test used to measure visual perceptual skills independent of motor ability and has norms for ages 2 through 18 years. Percentile scores are determined in comparison to the child’s age, with scores below the 10^th percentile indicating impaired visual-perceptual skills.

The WeeFIM [25], cognition and communication sub-section, was used in the form of a parent questionnaire to assess cognitive abilities. Scores range from 0 to 35 with higher scores indicating a higher level of cognition. Studies have found significant relationships between cognitive scores on the WeeFIM and standardized neuropsychological testing with verbal memory in particular in children with traumatic brain injury [26].

The Pediatric Evaluation of Disability Inventory (PEDI) [27] self-care domain was utilized to evaluate independence in self-care activities. This standardized assessment has norms for children from age 0 through 7 years, and can be used for a population of children with developmental disabilities until age 18. It has been found to be appropriate for assessing level of independence in children with MMC [28]. The overall standard score was calculated. In addition, individual scores on the upper and lower body dressing and bathing subtests were recorded from 0 (need full assistance) to 5 (completely independent).

2.3 Statistical analysis

All statistical analyses were performed using SPSS v. 22 software packages; p-value < 0.05 was considered statistically significant. Descriptive statistics included number and percentage, median and range or mean and standard deviation. Times for the 9HPT were compared to age and gender norms and the standard score was recorded as number of standard deviations above (slower performance) or below (faster performance) the norm [20]. Significant level was calculated by the one sample Wilcoxon non parametric test with an assumed median of 0 (based on norm Z scores distribution). The Mann Whitney U test was used for assessing differences in functional level between children with or without hydrocephalus. Associations between the 9HPT results and functional performance were determined using Spearman correlation coefficients. A linear stepwise regression analysis was performed with the standard score of the 9HPT for both the dominant and non-dominant hands as dependent variables.

2.4 Procedure

After obtaining parental consent, the assessments were administered during the participants’ annual clinic visits by the MMC multidisciplinary team. The 9HPT and Beery were administered by an experienced occupational therapist. The PEDI and WeeFIM were administered by an occupational therapist via an interview with the child’s parent. The sociodemographic questionnaire was completed by the parents and the clinic’s social worker.

3 Results

Ninety-four children participated in this study, ranging in age from 4 to 18 years (mean±SD =10.5±4.0). Other socio-demographic characteristics are presented in Table 1.

Table 1
Sociodemographic characteristics (N = 94)

Age (years mean±SD, range) 10.5±4.0, 3.5–18.1

Gender (number, %) Male 47, 50%

Educational setting (number, %)

Special 40, 42.6%

Regular 37, 39.4%

Integrated 17, 18.1%

Age (years mean±SD, range)

Father 43.7±8.8, 28–70

Mother 39.9±7.6, 28–56

Education (years mean±SD, range)

Father 10.5±4.6, 0–23

Mother 9.8±4.8, 0–19

Siblings (number, range) 5, 1–16

Mean family income (number, %)

Below average 51, 54.3%

Average 24, 25.5%

Did not respond 19, 20.2%

Approximately 85%of the children with hydrocephalus (72) had a shunt (Table 2). Since only one did not have Arnold Chiari, the current use of the term hydrocephalus includes Arnold Chiari. Children with hydrocephalus had a significantly higher mean functional neurological level (median L2, range T2-S3) than children without hydrocephalus (median L4, range L3-S2) (p < 0.01).

Table 2

Subjects’ lesion characteristics

	Number	%
Functional neurological level
High thoracic (T2-T6)	3	3.2
Low thoracic (T7-T12)	33	35.1
High lumbar (L1-L3)	22	23.4
Low lumbar (L4-L5)	19	20.2
Sacral	17	18.1
Hydrocephalus	85	90.2
Hydrocephalus with a shunt	72	76.6
Arnold Chiari	84	89.4

Almost all had received occupational therapy and/or physical therapy treatment in the past or were receiving therapy at the time of the study. This potentially confounding factor was not considered relevant to the analysis. Twenty-five percent were left hand dominant and six (6.4%) did not have a clear hand dominance. Their scores on the fine motor dexterity 9HPT were significantly greater than the age-normed mean values, i.e., relative to their typically developing peers. It took the children in this study longer to perform (median dominant hand Z score = 4.1 (p < 0.001) and median non-dominant hand Z score = 4.5 (p < 0.001) as shown in Table 3.

Table 3

Main and secondary outcomes (N = 94)

	Median	Minimum-
Maximum
Main outcome
Standard score of the 9HPT (dominant)	4.1	0.1–18.7
Standard score of the 9HPT (non-dominant)	4.5	0–19
Secondary outcomes
WeeFIM (cognition - range 5–35)	33	13–35
Visual-Motor Integration (Beery in percent)	7	0–94
PEDI sub scores
Bathing (sub item rate range 0–5)	2	0–5
Dressing upper body (sub item rate range 0–5)	2	0–5
Dressing lower body (sub item rate range 0–5)	1	0–5

The functional neurological level of MMC, presented as an interval variable, e.g. T1 = 1, T2 = 2 . . . . L1 = 13 was found to have a moderately significant positive association with the standard score of the 9HPT in the dominant hand but not in the non-dominant hand, i.e., a child with a higher functional neurological level took longer to complete the 9HPT with the dominant hand.

A negative weak but significant association was found between the standard score on the 9HPT with both hands and lower body dressing as shown in Table 4.

Table 4

Significant correlations between standard score of the 9HPT and child and parents’ characteristics and child functional performance

	Standard score of the 9HPT
	Dominant	Non-dominant
Child characteristics
Age		0.31^**
Functional neurological level	0.43^**
Shunt number		0.27^*
Years of parental education
Father		–0.30^*
Mother		–0.25^*
Child’s functional performance
VMI (Beery)	–0.23^*	–0.35^*
WeeFIM (cognition)	–0.25^*	–0.33^*
PEDI sub-item (Dressing lower body)	–0.22^*	–0.22^**

^*p < 0.05, ^**p < 0.01; VMI = Visual-Motor Integration; PEDI =Pediatric Evaluation of Disability Inventory

Weak correlations were found between 9HPT scores and cognitive levels, perceptual skills, and demographic variables. Children with a higher cognitive level according to the parental report on the WeeFIM and those with higher scores on the Beery visual perceptual test performed the 9HPT faster with both hands.

The child’s age was correlated with 9HPT scores in the non-dominant hand, i.e., the older the child, the longer time it took to perform the task compared to norms for others in their age range. Both father’s and mother’s years of education were found to have a significant negative association with the standard score of the 9HPT in the non-dominant side, i.e., children with more educated parents performed the test faster with the non-dominant hand. No significant associations were found between hand function and other personal or environmental factors such as gender, number of siblings, economic level and educational setting.

Lastly, a stepwise linear regression model was performed with the standard score of the 9HPT scores for both the dominant and non-dominant hands as dependent variables. The child’s age, cognitive level, having a shunt, mother’s age and years of education were the independent variables that remained in the model for the non-dominant hand. The model explained 48%of the variance in the standard score of the 9HPT for this hand. The only factor that remained in the model in the dominant side was lesion level (Table 5).

Table 5

Linear regressions; NHPT as dependent

	B	Std. Error	t-value	p-value	Partial R²
Standard score of the NHPT (non-dominant)
Age	0.81	0.15	5.27	< 0.001	0.14
WeeFIM-cognition	–0.60	0.13	–4.62	< 0.001	0.20
Mother’s age	–0.28	0.08	–3.44	0.001	0.06
Mother’s years of education	–0.31	0.12	–2.81	0.006	0.05
Shunt	2.45	1.17	2.09	0.040	0.03
F5;68 = 12.52, p < 0.001, R² = 0.48
Standard score of the NHPT (dominant)
Functional neurological level	0.33	0.09	–3.84	< 0.001	0.17
F1:73 = 14.73, p < 0.001, R² = 0.17

4 Discussion

Children with MMC have significantly poorer hand dexterity skills than their typically developing peers of the same age and gender.

Similar to Turner’s [19] sample, a much larger percentage of children in the current study were left hand dominant (25%based on parental report) which is much more prevalent than the 5–10%found in the average population approximately [29]. In addition, hand dominance for approximately 6%of the children in the current study was not evident. This may be due to the association of hydrocephalus with non-dextrality or that children with MMC and hydrocephalus exhibit a delayed establishment of hand dominance [30]. In typically developing children, hand dominance is generally established by the age of 5 or 6 years, with hand preference emerging as early as infancy, and most children demonstrating a clear hand preference by the age of 3 years [31]. Hydrocephalus may lead to early damage of the left hemisphere in children who would otherwise develop right hand dominance, causing them to switch to a left hand preference, thus resulting in a less skilled dominant left hand [32]. In this study, certain factors were associated with function in the dominant hand and other factors were associated with function in the non-dominant hand, perhaps due to some ambiguity in their true dominance.

The factors most related to hand dexterity in children with MMC were their functional neurological level, having a shunt, the child’s age and cognitive level and the mother’s age and years of education. Our findings are similar to Jansen et al.’s [13] demonstration of a significant correlation between hydrocephalus and shunt with poor hand function.

Hand dexterity scores were not associated with most areas of self-care. However, better scores were associated with greater independence in lower extremity dressing, a finding likely related to their very limited lower extremity function which would require greater compensation by their fine motor abilities. This is in accordance with the relationship we found between functional neurological level and hand function. Since a higher level of lesion indicates poorer postural control, it is likely that children with a higher functional neurological level would have more difficulty with fine motor skills, which would be dependent on a stable base of support in the trunk [18]. Lower extremity dressing is generally dependent on efficient postural control, therefore, impairments in both postural control and hand function would make this task more difficult to perform.

The 9HPT is a tool that measures speed in a task requiring dexterity. The relationship between 9HPT scores and cognitive level may be attributed to the reduced speed of the children who were more impaired cognitively. This appears to be consistent with other studies that found that individuals with MMC with slower cognitive processing took a longer time to complete hand function tests [13]. In addition, it is possible that the weak association found between the 9HPT and scores in lower extremity dressing on the PEDI self-care scale is related both to motor deficits and to difficulties in cognitive processing skills which can result in slow performance of motor tasks in children with MMC [9 , 30].

As children with MMC get older, it appears as though their skills and abilities increasingly lag behind their typically developing peers. Given the challenges individuals with MMC face and the negative impact on their quality of life which seems to decline with age [33, 34], it is essential that therapy continue past childhood into their teen years and even as they transition to adulthood. Environmental factors such as the influence of years of maternal education, as shown in the current study, may point to the need to adapt instructional materials so that they are understandable to the families regardless of their educational level. It is possible that mothers who are more educated understand the importance of playing with their children and encouraging them to participate in fine motor activities, thus improving their hand dexterity. Since the family’s participation is critical in promoting the child’s function, materials need to be delivered in a way such that each particular family may benefit.

Hand dexterity is necessary for function, for example, the ability to perform self-care activities [21], self-catheterization [35], and ambulation in children with MMC [36] and for academic performance such as handwriting [37]. Therefore, it is imperative that children with MMC develop their hand dexterity skills, even as they get older, especially considering that they often need to compensate for decreased lower extremity function via their hand skills. In addition, a thorough evaluation of fine motor skills in children with MMC may contribute to planning effective interventions to address independence in self-care activities such as dressing, bathing and catheterization. For example, therapists may need to consider adaptations for managing bowel and bladder, for dressing, or to substantiate a recommendation of keyboarding as an alternative to handwriting. The results of the current study reinforce the importance of addressing hand dexterity when treating individuals with MMC.

4.1 Limitations

The only measure of hand function utilized in this study was the 9HPT. Employing more extensive measures of it, such as hand strength, fine motor control and precision, and coordination would provide a more in-depth investigation of hand function in children with MMC. In addition, due to time constraints, cognitive level was assessed via the WeeFIM as obtained from subjective parental reports. The use of this rapid screening tool limits definitive conclusions regarding cognitive impairment; additionally, more comprehensive testing of cognitive impairment is recommended. Finally, some of the subjects were receiving occupational therapy treatment for hand skills at the time of the study which may have affected their results on the 9HPT.

5 Conclusions

This is the most recent study to investigate the relationship between hand dexterity in a large sample of children with MMC along with factors related to the disease and the child’s personal characteristics, environment, and function. While therapists do not influence the primary impairments of MMC, they are able to reduce its secondary impairments. Thus, identification of the relationships related to age, need for support in lower extremity dressing and parental education supports the setting of key clinical objectives. Our results strengthen the significance of improving hand dexterity and continuing to do so as the children get older. In addition, providing parent education in fine motor games and activities that they can play with their children at home, and adapting these activities to each family’s educational level may help improve hand dexterity and functional goals. Further studies focusing on interventions designed to improve fine motor function and to minimize the effects of such impairments on independence in self-care activities in children with MMC are recommended.

Footnotes

Acknowledgments

We would like to thank the children and parents who participated in the study, the clinic staff, Coos Wever, Adi Bracha Baron, and Levana Shoshan for assisting with evaluations, and Nurit Tvil for technical assistance. Funding for the study was provided by ALYN Pediatric and Adolescent Rehabilitation Center.

Conflict of interest

The authors have no conflicts of interest to report.

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Age (years mean±SD, range)	10.5±4.0, 3.5–18.1
Gender (number, %)	Male 47, 50%
Educational setting (number, %)
Special	40, 42.6%
Regular	37, 39.4%
Integrated	17, 18.1%
Age (years mean±SD, range)
Father	43.7±8.8, 28–70
Mother	39.9±7.6, 28–56
Education (years mean±SD, range)
Father	10.5±4.6, 0–23
Mother	9.8±4.8, 0–19
Siblings (number, range)	5, 1–16
Mean family income (number, %)
Below average	51, 54.3%
Average	24, 25.5%
Did not respond	19, 20.2%

Exploring hand dexterity in children with myelomeningocele

Abstract

PURPOSE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1 Introduction

2 Methods

2.1 Participants

2.2 Instruments

2.3 Statistical analysis

2.4 Procedure

3 Results

4.1 Limitations

5 Conclusions

Footnotes

Acknowledgments

Conflict of interest

References