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Changes in elementary finger–hand functions over time in preschool children with spastic cerebral palsy
Neuroscience Letters 455 (2009) 30–35
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Changes in elementary finger–hand functions over time in preschool children with spastic cerebral palsy R. Blank a,∗ , G. Kluger b a b
Child Centre Maulbronn and University of Heidelberg, Knittlinger Steige 21, 75433 Maulbronn, Germany Neuropediatric Department, BHZ Vogtareuth, Vogtareuth, Germany
a r t i c l e
i n f o
Article history: Received 1 December 2008 Received in revised form 14 March 2009 Accepted 18 March 2009 Keywords: Grip force Tapping Children Corticospinal lesion Cerebral palsy
a b s t r a c t To examine the development of basic finger–hand motor capacity in a one-year follow-up experiment performed on young children with bilateral spastic cerebral palsy (CP). The maximal finger grip strength (FGMAX), the frequencies of the fastest voluntary isometric finger force changes (FGCHANGE) while holding an object, in addition to the finger (FTAP) and hand tapping frequencies (HTAP) were examined on two separate occasions in 30 children between the ages of three to six years with bilateral spastic CP (BCSP). The examinations were performed 12 months apart in order to test for improvements in the aforementioned functions. After a one-year period of time, the FGMAX, FGCHANGE and FTAP values increased by 10–15% in both hands (changes in FTAP values were not statistically significant), while the HTAP values remained unchanged. In regard to the normative samples obtained from children of this age period, the gap in the motor capacity of the fingers did not increase. We observed an improvement in the basic finger functions over a one-year period of time in preschool aged children diagnosed with spastic CP. Interestingly, the improvement proceeded at a similar rate to that observed in normally developing children. However, the fastest hand tapping movements (HTAP) did not improve during this one-year time interval. In addition, we observed that in young children with BSCP, there appears to be considerable potential for the development and reorganisation of the elementary finger functions that are requisite for object manipulation. © 2009 Elsevier Ireland Ltd. All rights reserved.
The development of the fastest repetitive voluntary motor activity as assessed for different types of movements including fastest repetitive tapping movements, aiming movements and a pegboard transportation task has been shown to accurately reflect the maturation of the fastest cortico-motoneuronal efferents [11]. Furthermore, the development of central conduction times has been thought to influence the speed of repetitive movements in children. However, it has been observed that no significant improvements in the speed of these movements occurred when these movements were trained over a period of two consecutive days [11]. The development of fastest voluntary movements was therefore interpreted as a structure-bound phenomenon that was independent from learning. If this hypothesis is true, then children who are subjected to lesions in the cortico-motoneuronal efferents should demonstrate a massive slowing of the fastest voluntary movement. In children, the most common movement disorder, which also serves as one of the best “human models” to examine the role of early acquired lesions of the corticospinal
∗ Corresponding author. Tel.: +49 7043 16171; fax: +49 89 71009148. E-mail address: [email protected] (R. Blank). 0304-3940/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2009.03.058
pathways and their reorganisation, is a disorder known as bilateral spastic cerebral palsy (BSCP). Most children with BSCP have a periventricular lesion in the corticospinal pathways that had been acquired during the third trimester of pregnancy (the so-called “periventricular leucomalacia”). Some children have inherited malformations of the brain. The extent of damage caused by the lesion appears to be correlated with the functional severity of the disorder [15]. Since the corticospinal tract is particularly important for hand motor functions, the careful examination of the finger–hand motor capacity is of significant interest. Indeed, children with BSCP demonstrate a massive slowing of their fastest grip force changes and low grip strength [3]. The important issue of whether or not this reduction in motor capacity is stable over time remains unresolved; however, this issue is important since the lesion usually occurs during the third trimester of pregnancy. In a 13-year follow-up study, the grip-lift synergy was recorded in children with BSCP during the task of lifting an object [8]. The children in this study, who were between the ages of 6 and 8 years old, showed considerable improvement, with some individuals demonstrating a normalization of the grip-lift synergy values in comparison to normal experimental subjects after the long-term
R. Blank, G. Kluger / Neuroscience Letters 455 (2009) 30–35
follow-up study. These results indicated that object manipulation can be improved without specific training over a long period of time. In addition, Duff and Gordon showed that even short-term repetitive training may improve the grip-lift synergy values [7]. However, grip-lift synergy is not only dependent on basic motor capacity but is also dependent on neuro-cognitive (such as the use of visual cues) and coordinative functions (such as the parallel programming of distal and proximal muscles of the upper extremities). From these studies, the question arises as to whether or not the grip-lift synergy has improved due to “unspecific” motor learning that occurs each day in an individual’s life or develops as a consequence of the maturation or reorganisation of the fastest cortico-motoneuronal efferents. Blank et al. showed that an intensive training period involving activities inherent to daily living may indeed change coordinative hand functions such as the grip-lift synergy but does not change basic motor capacity, such as the maximum tapping frequency or grip strength [5], which is in accordance with the observations reported by Muller and Homberg in normally developing children. This indicates that the impairment of basic motor capacity such as weakness (reduced grip strength) and spasticity (impaired ability in rapid movements or in grip force changes) is typical for corticospinal damage whereas lifting requires additional coordinative abilities and motor programming, which may be learned by performing everyday activities or by the implementation of training periods over time [7,17]. In addition, it is known that the gross motor function of cerebral palsy patients (GMFCS levels I–III) about 80–90% of the children reach their highest level of gross motor function between 5 and 7 years of age [6,13,18]. Therefore it is unknown whether or not there is any improvement or deterioration in the basic finger–hand functions in children with CP. Knowledge of such information may influence the potential for changes in function and activities over time. The motor capacity of the finger–hand functions is considerably improved in preschool-aged children. The most manipulative skills relevant to activities necessary for daily life appear to be acquired the same way in normally developed children as they are in children with cerebral palsy, during their respective life spans. Thus, it is of particular interest to understand if and how children of this age group who have been diagnosed with BSCP can alter their basic force and movement functions. The objective of the present longitudinal study was to examine the development of elementary finger and hand functions, including the finger (FTAP) and hand tapping (HTAP) values, the fastest isometric finger grip force changes (FGCHANGE) and the maximum grip strength (FGMAX) in children between the ages of three to six years old with spastic CP. The specific experiments involved the determination of whether there were general improvements or impairments in the basic motor capacity values of individuals over time, and whether these changes were different in CP children compared to normally developing children of the same age-group. These variables should be examined after a one year period without “specific” training, which means without the implementation of training sessions for tapping, grip strength and isometric force changes in the absence of medical treatment, since, for example, botulinum toxin is one drug known to influence these motor functions. We examined the longitudinal change in the following basic finger–hand functions: 1. The FGMAX and FGCHANGE values were measured in order to evaluate basic finger force functions. The forces were measured using an instrumented object (height × depth × width of 90 mm × 40 mm × 30 mm, weighing 200 g) containing a uniaxial force sensor that measured the grip force (0–100 ± 0.2 N)
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Fig. 1. The target variables of the fastest isometric force changes (frequency [Hz] = 1000/(duration of force increase + force decrease [ms])).
exerted against the grasping surface.1 The instrument was held using a hand precision grip with the thumb and digits 2 through 5 in an appropriate opposition. 2. The FTAP and HTAP values were determined to analyse the fastest finger and hand movements. For this set of experiments, a 3D movement analysis system (ultrasound based) was implemented.2 This analysis involved the use of an active marker system with small markers on the hand that transmit ultrasound waves to a receiver. Upon receiving the signals, the markers could easily be analysed and the temporo-spatial variables could then be calculated. The markers were placed on the nail of the index finger, over the joint between the index finger and the hand, and over the joint of the wrist of the hand (middle). The patients performed the standardized tasks using their preferred and their non-preferred hands separately. Hand preference was determined by observation of activities inherent to daily living (modified to Salmaso and Longoni [14]. In addition, the children were instructed to perform the following tasks: 1. In the FGMAX experiments, the children were instructed to press the box as often as possible (“squeeze out like an orange”). The children had at least 3 trials, with each trial lasting 20 s, in order to ensure understanding of the experimental parameters and in order to prevent fatigue. Within this observation period, the maximum grip force (best performance) was used for analysis. 2. In the FGCHANGE experiments the children were instructed to increase and decrease (press and release) their grip force while holding the box as often as they could within a time period of 20 s. In order to ensure that the children understood the task, the children could see their actual grip force increasing and decreasing on a computer screen (no tracking of a visual cue was used and the target variables are displayed in Fig. 1). 3. In the FTAP experiment, the children were instructed to tap on a table using their index finger as quickly as possible. In this set of experiments, the target variable was the tapping frequency. The dimension of the measurement was the number of movements per second.
1 Manufacturer: Research Group Clinical Neuropsychology, Clinical Center of Bogenhausen, Munich, Germany. 2 Zebris Medical GmbH, Max-Eyth-Weg 42, D-88316 Isny im Allgäu, E-mail: [email protected].
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4. In the HTAP experiments, the children were instructed to tap on the table with their hand as quickly as possible. In this set of experiments, the target variable was the tapping frequency. The dimension of the measurement was the number of movements per second. In order to ensure that the children understood the experimental setup and in order to minimize the training effects, the children were instructed to practice each test. In order to minimize the effects of fatigue and motivation, only the fastest five periods were used for statistical analysis in tasks two to four. Since we used only short test periods and evaluated only the best performance from each child, the results are not likely to be influenced by fatigue. Overall, a total population of 30 children, which consisted of 22 boys and 8 girls (5 three-year olds, 11 four-year olds, 12 fiveyear olds, 2 six-year olds) and included 20 children preferred using their right hands and 10 children preferred using their left hands in activities of daily living (e.g. playing, eating). All of these children were diagnosed with BSCP according to the criteria established by the Surveillance of Cerebral Palsy in Europe (SCPE) and were examined two separate times, with a period of 12 months between each examination [1]. Hand laterality was assessed by the observation of activities inherent to daily living that could be performed by each child. The severity of each test was classified according to the Manual Ability Classification System (MACS) [9] that included the following criteria (three levels of severity): I. The ability to handle objects easily and successfully. At most, there may be limitations in the ease of performing manual tasks that require speed and accuracy. However, any limitations in these manual abilities do not restrict the independence of performing daily activities. II. The ability to handle most objects with somewhat reduced quality and/or speed of achievement. Here, certain activities may be avoided or may be performed with some difficulty. In addition, alternative ways of performing a task may be used but manual abilities do not usually restrict the independence of performing daily activities. III. The ability to handle objects with difficulty. Here, children need help preparing and/or modifying activities. Their performance is slow and achieved with limited success in regard to the quality and quantity of the performance. The activities could be performed independently if they were previously arranged or had been adapted. The MACS levels were distributed among level I 8, level II 11, and level III 11. During the one-year period of the experiment, the children received no therapy aiming to improve basic motor capacities such as strengthening or anti-spastic treatments. This could be controlled as all children would have needed prescriptions by medical doctors for such therapies. The quality and quantity of general interventions were equivalent to those being described in detail in Blank et al. [5]. The children repetitively practiced everyday activities within a Conductive Education program (three blocks of four weeks) and further low intensity standard programs that were typical for children of this age group. In this previous study, even the high-intensity intervention has failed to show any effects on basic motor activities like FGMAX, FGCHANGE, FTAP and HTAP [5]. Furthermore, we examined the changes in the relationship between normally developing children and children with BSCP of the same age, in order to predict whether or not the differences in the measured variables between children with BSCP and normally developing children increases or decreases. Thus, we performed an age-normalised comparison with a reference sample of
normally developing children. These data were transformed into age-corrected values (“z-values”), which were based on a sample of 125 normally developing children between the ages of three and six years old with no history of therapy, no neurological abnormalities, and no deficits in everyday function. Neurological impairments, especially fine motor problems were excluded by history and by clinical examination according to Touwen [16]. These normally developing children were gathered from two kindergarten classrooms and served as standardization samples. The z-values for the children with BSCP were calculated using the individual value of the child with BSCP minus the mean standard value determined from the children of the corresponding healthy age group. This was then divided by the standard deviation of the mean value of the healthy corresponding age-group. For example, a z-value of +2.1 indicates that the child had a value that was 2.1 standard deviations above the mean of a normal child from the same age, thus indicating greater than 2 standard deviations, or in other words, a value that is above 97.5% of the reference sample of the same age. On the other hand, a z-value of −2.3 indicates that the child had a value that was 2.3 standard deviations below the average value obtained from a normal child of the same age, thus indicating greater than 2 standard deviations below the mean of a normally developed child of the same age (below 2.5% of the reference sample). The follow-up examination, which occurred 12 months later, was evaluated using t-tests for dependent samples (each child served as own control that means data of the first and second tests were dependent from each other). In a second analysis, all children that could not be examined on both occasions or dropped out in one test because of specific difficulties (e.g. finger tapping appeared to be more difficult than maximum grip force) received the same values as their other examination (effect was set as zero effect). Children that could not perform a test twice receive the mean value of all other children during the first examination at both examinations (again effect was set to zero). The examination was performed within a playful setting and within the usual diagnostic setting. The ethical principles outlined in the Declaration of Helsinki were followed. For statistical analysis, the Statistical Package SPSS, Version 12.0 was used.3 Data before and after 12 months were obtained from 28 children for FGMAX, from 27 children FGCHANGE, from 26 children for FTAP, and from 21 children for HTAP (preferred hands). The significant decrease in the number of children analysed via the HTAP test was a consequence of the fact that six children (n = 1 for MACS level I, n = 1 for MACS level II, and n = 4 for MACS level III) during the first examination, and four children one year later (n = 1 for MACS I, n = 2 for MACS II, and n = 1 for MACS III) were not able to perform the task according to the instructions. In regard to the use of the non-preferred hands, the drop-out rate was much higher. After completing both examinations, data could only be analysed for 13 children in the FGMAX analysis, for 9 children in the FGCHANGE analysis, for 5 children in the FTAP analysis, and for 7 children in the HTAP analysis. Thus, the results of the non-preferred hands cannot be interpreted due to a lack of sufficient data. Nevertheless, the drop-out analysis showed that drop-out rates were higher for the first examination than for the second examination that suggested some improvement in these motor skills (drop-outs of the first examination versus the second examination include n = 10 for the FGMAX first examination versus n = 9 for the second examination, n = 16 for the FGCHANGE first examination versus n = 11 for the second examination, n = 24 for the FTAP first examination versus n = 9 for the second examination,
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SPSS Inc. Headquarters, Corporate Headquarters, 233 S Wacker Drive, Chicago,
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and n = 22 for the HTAP first examination versus n = 9 for the second examination). Within one year, the values of the FGMAX analysis improved considerably from (means) 27.8N (SD 11.4) to 34.5 N (SD 11.6) (t = −3.4, p < 0.001) for the preferred hands and from 23.8N (SD 7.0) to 26.9 N (SD 8.5) (t = (2.7, p < 0.001) for the non-preferred hands (Fig. 2). The values for the FGCHANGE analysis also improved significantly for the preferred hands, increasing by approximately 15% from the mean value of 1.5 Hz (SD 0.60) to 1.8 Hz (SD 0.57) of force change per sec (t = 3.9, p < 0.001). In regard to the non-preferred hands, there was an improvement of approximately 10% (1.30 Hz (SD 0.46) to 1.43 Hz (SD 0.38)) but these values were not statistically significant due to the small number of children being able to perform the test using their non-preferred hands (Fig. 2). In addition, the values for the FTAP analysis improved by roughly 10% (mean frequency and standard deviation (SD) values for the preferred hand increased from 1.73 Hz (0.55) to a value of 1.91 Hz (0.43) while these values also increased for the non-preferred hand from 1.77 Hz (0.51) to 1.86 Hz (0.60)). However, due to the variability of the group sizes, the changes were not statistically significant. Interestingly, the values for the HTAP analysis did not show a statistically significant increase (the mean values (SD) for the frequencies of the preferred hand increased from 1.97 Hz (0.58) to 1.98 Hz (0.52) while the mean values for the non-preferred hand increased from 1.48 Hz (0.75) to 1.56 Hz (0.58), which was not significant here). If the drop-outs were included by setting their effects to zero the results were as follows (preferred hands): FGMAX: T0 29.69N (SD 9.81), T12 34.36N (SD 9.81), t = 3.7, p < 0.001, FGCHANGE: T0 1.59 (SD 0.49), T12 1.9 (SD 0.51), t = 4.2, p < 0.001, FTAP: T0 1.73 (SD 0.59), T12 1.86 (SD 0.50), t = 1.3, n.s., HTAP: T0 1.85 (SD 0.47), T12 1.94 (SD 0.47), t = 1.2, n.s. This means all basic motor functions improved; however, finger and hand tapping became not significant because of higher variation and slightly lower mean changes. Because of high drop-outs and high variation of the data the results on the non-preferred hands can only be interpreted in a descriptive way e.g. by comparing the drop-out rates on both exam-
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inations. A quantitative analysis by alluding missing data to zero effect seemed to be not sensitive. When these results are transferred to the age-related changes observed in normally developing children, the improvement in the force parameters indicated that the gap between normal children and children with CP decreased slightly, however this decrease was not statistically significant (Fig. 3). This indicates that the age-related changes in both normally developing children and in children with CP were similar. In regard to the finger movement velocities, the gap between normally developing children and children with CP remained approximately equivalent (Fig. 3). These results indicated that the changes related to age were similar upon comparison to normally developing children. Thus, within a time period of one year, the elementary motor functions of the fingers of preschool children with BSCP improved by 10–15%. This rate of change is similar to the rate of change observed in normally developing children. This increase is relevant since these changes are the basis for relevant improvements in the activities inherent to daily living as observed in preschool children. In addition, we conclude that the HTAP values did not change over the one-year period of time analysed in this study. Longitudinal changes in the capacity of basic finger and hand motor skills were examined in children between the ages of three and six years olds. Hand tapping was most difficult task for the children to perform since it dealt with the hand and not with the entire arm. The drop-out analysis shows that drop-outs are less common in the second set of examinations. This is consistent with our observation of general improvement. Further, “zero-correction” of missing data did not change the general results. Therefore, concerning the results on the preferred hands we are quite confident that the drop-outs do not influence the general results. The results on the non-preferred hands also indicate improvements but cannot be interpreted quantitatively in comparison with the preferred hands because of a high proportion of drop-outs. The results presented herein indicate that the relevant development of fine motor functions is usually observed within a one-year period in this age group. It is important to point out that the lesions or malformations of the corticospinal tract that resulted in children having BSCP had likely occurred during the third trimester of pregnancy.
Fig. 2. The development of maximum grip force and fastest isometric force changes in children between the ages of 3–6 years old with bilateral spastic cerebral palsy within one year (preferred and non-preferred hands) where T0 = first examination, T12 = second examination after 12 months; **p < 0.01, *p < 0.05, ◦ p = 0.06.
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Fig. 3. The age-corrected comparison of the development of the elementary finger–hand functions (maximum grip force, fastest isometric force changes, finger and hand tapping frequency) in children between the ages of 3–6 years old with bilateral spastic cerebral palsy within one year as compared to the development of a normal children of the same age (mean ± standard deviation is z = 0 ± 1 based on a population of 125 normal children), where T0 = first examination, T12 = second examination after 12 months, and n.s. = not significant).
A major unresolved issue involves whether or not these improvements in motor functions over time are caused by structural changes of the moto-neurocortical network (such as “maturation,” which is an intrinsic effect) or by therapeutic interventions (such as “environmental effects”, which are extrinsic effects). For ethical reasons, therapeutic intervention was required over a significantly long time interval. We cannot completely exclude the possibility that environmental (therapeutic) factors interfered with these results. This situation invokes a kind of nature-nurture problem. However, we believe that there is some evidence from previous studies indicating that intrinsic effects may mainly be responsible for such observations. Muller and Homberg have previously shown that the development of basic motor capacity in normally developing children is related to structural changes that occur in the moto-corticospinal efferents [11]. An intensive training period involving elementary finger–hand functions, such as tapping, performed on two consecutive days did not show any significant improvement. In addition, Duff et al. have shown that in contrast to basic motor capacity such as lifting an object, a coordinative function can be improved in children with CP within a short period of time that involves repetitive training.
In addition, a study by Blank et al. supports both of the aforementioned findings [5]. Indeed, Blank et al. have shown in an A–B–A study that within a nine-month period involving intensive training activities inherent to daily living (7 h a day), it is possible to improve coordinative functions such as lifting (as reported by Eliasson), but there was no additional effect of intensive therapy on basic finger–hand functions (tapping, grip strength, etc.) when compared to phases without intensive training. As the children in the present study received equivalent therapeutic input to the previous study [5] we can assume that the changes of basic motor capacity over time are not caused by training effects. The data presented herein show that, in spite of the lesions to their moto-corticospinal efferents, children with BSCP can improve their finger grip strength, finger movement velocity and maximum isometric finger force rates by 10–15% within a one-year period. In addition, the similar rate of change over time also observed in normally developing children leads to the hypothesis that a certain amount of intact moto-neuronal efferents and networks may be responsible for these positive changes. The motor capacity of the fingers appears to improve particularly in this age group without specific strength training or training of the elementary finger–hand movement by invoking exercises such as tapping.
R. Blank, G. Kluger / Neuroscience Letters 455 (2009) 30–35
On the basis of the studies mentioned, we believe that the significant improvements of coordinative functions such as lifting, as reported by Eliasson et al. after a 13-year period, should be interpreted by developmental effects on the basis of structural changes to the intact moto-neurocortical networks (intrinsic changes) in addition to training effects (extrinsic changes) [8]. The second finding of our study was that more proximal functions such as the velocity of wrist flexion and extension during hand tapping did not improve within this period of observation. However, one needs to be very careful with further interpretations because of the high drop-out rate in the hand tapping task. It seems that children with BSCP below six years of age have more potential to improve distal motor functions than more proximally generated movements. In addition, different developmental profiles for finger and hand movements have also been shown, for example, in the process of drawing with a pencil in normally developing children [4]. So far, there are no longitudinal studies focused on hand motor functions in children with CP that address the changes over time within and between certain severity levels classified by the MACS. For gross motor functions, high stability over time was found and even “gross motor function curves” could be established [12]. Beckung et al. and Hanna et al. showed that most children with spastic CP reached their “peak” performance between the 5th and 7th anniversary although there may be some variability between the gross motor development of children with CP [2,10]. This means that the differences in gross motor functions between normal developing children and children with CP steadily increase during kindergarten age. This is in accordance with early studies involving the walking prognosis of children with CP [6,13,18]. The present findings indicate that the prognosis of fine motor capacity may be better. The different development of the finger motor functions as compared to the proximal or gross motor functions may be explained by the nature of the periventricular lesions in children with CP. The corticospinal pathways to the fingers are more distant from the periventricular area than those to the lower extremities and therefore, they may be less affected by periventricular lesions in children with spastic cerebral palsy. On the other hand, the input of cortico-motoneuronal efferents that control the finger function is particularly important and it is likely that a number of efferents may still be intact in order to procure the normal pattern of development, but the number of intact efferents may not be sufficient to achieve normal finger strength and velocity. The results of this study may thus have important therapeutic implications. The specific improvement of the basic finger motor functions in children with BSCP may suggest that there may be potential for intensive therapeutic approaches in specifically improving finger–hand functions, as opposed to gross motor functions. In conclusion, this study supports the hypothesis that in young children with BSCP, the basic motor capacity of the finger functions considerably improves during preschool years in spite of the
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presence of the lesions. Studies examining the long-term effects of therapeutic interventions on finger–hand functions in children of this age should take into consideration these changes over time. Acknowledgement We wish to thank to the clinical and laboratory staff of the Department of Sensomotor Functions of the Child Centre Munich that supported the examination of the children within the clinical setting. References [1] Surveillance of cerebral palsy in Europe: a collaboration of cerebral palsy surveys and registers. Surveillance of Cerebral Palsy in Europe (SCPE), Dev. Med. Child Neurol. 42 (2000) 816–824. [2] E. Beckung, G. Carlsson, S. Carlsdotter, P. Uvebrant, The natural history of gross motor development in children with cerebral palsy aged 1 to 15 years, Dev. Med. Child Neurol. 49 (2007) 751–756. [3] R. Blank, J. Hermsdorfer, Basic motor capacity in relation to object manipulation and general manual ability in young children with spastic cerebral palsy, Neurosci. Lett. 450 (2009) 65–69. [4] R. Blank, V. Miller, H. von Voss, R. von Kries, Effects of age on distally and proximally generated drawing movements: a kinematic analysis of school children and adults, Dev. Med. Child Neurol. 41 (1999) 592–596. [5] R. Blank, R. von Kries, S. Hesse, H. von Voss, Conductive education for children with cerebral palsy: effects on hand motor functions relevant to activities of daily living, Arch. Phys. Med. Rehabil. 89 (2008) 251–259. [6] A.C. Da Paz junior, S.M. Burnett, L.W. Braga, Walking prognosis in cerebral palsy: a 22-year retrospective analysis, Dev. Med. Child Neurol. 36 (1994) 130–134. [7] S.V. Duff, A.M. Gordon, Learning of grasp control in children with hemiplegic cerebral palsy, Dev. Med. Child Neurol. 45 (2003) 746–757. [8] A.C. Eliasson, H. Forssberg, Y.C. Hung, A.M. Gordon, Development of hand function and precision grip control in individuals with cerebral palsy: a 13-year follow-up study, Pediatrics 118 (2006) e1226–e1236. [9] A.C. Eliasson, L. Krumlinde-Sundholm, B. Rosblad, E. Beckung, M. Arner, A.M. Ohrvall, P. Rosenbaum, The Manual Ability Classification System (MACS) for children with cerebral palsy: scale development and evidence of validity and reliability, Dev. Med. Child Neurol. 48 (2006) 549–554. [10] S.E. Hanna, P.L. Rosenbaum, D.J. Bartlett, R.J. Palisano, S.D. Walter, L. Avery, D.J. Russell, Stability and decline in gross motor function among children and youth with cerebral palsy aged 2 to 21 years, Dev. Med. Child Neurol. (2009), doi:DMCN3196 [pii] 10.1111/j.1469-8749.2008.03196.x. [11] K. Muller, V. Homberg, Development of speed of repetitive movements in children is determined by structural changes in corticospinal efferents, Neurosci. Lett. 144 (1992) 57–60. [12] R.J. Palisano, D. Cameron, P.L. Rosenbaum, S.D. Walter, D. Russell, Stability of the gross motor function classification system, Dev. Med. Child Neurol. 48 (2006) 424–428. [13] A. Sala, D. Grant, Prognosis for ambulation in cerebral palsy, Dev. Med. Child Neurol. 37 (1995) 1020–1026. [14] D. Salmaso, A.M. Longoni, Problems in the assessment of hand preference, Cortex 21 (1985) 533–549. [15] A. Soot, T. Tomberg, P. Kool, R. Rein, T. Talvik, Magnetic resonance imaging in children with bilateral spastic forms of cerebral palsy, Pediatr. Neurol. 38 (2008) 321–328. [16] B. Touwen, The Neurological Examination of the Child with Minor Nervous Dysfunction, Georg-Thieme Verlag, Stuttgart, New York, 1982. [17] D.V. Vaz, M. Cotta Mancini, S.T. Fonseca, D.S. Vieira, A.E. de Melo Pertence, Muscle stiffness and strength and their relation to hand function in children with hemiplegic cerebral palsy, Dev. Med. Child Neurol. 48 (2006) 728–733. [18] E. Wood, P. Rosenbaum, The gross motor function classification system for cerebral palsy: a study of reliability and stability over time, Dev. Med. Child Neurol. 42 (2000) 292–296.
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Changes in elementary finger–hand functions over time in preschool children with spastic cerebral palsy R. Blank a,∗ , G. Kluger b a b
Child Centre Maulbronn and University of Heidelberg, Knittlinger Steige 21, 75433 Maulbronn, Germany Neuropediatric Department, BHZ Vogtareuth, Vogtareuth, Germany
a r t i c l e
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Article history: Received 1 December 2008 Received in revised form 14 March 2009 Accepted 18 March 2009 Keywords: Grip force Tapping Children Corticospinal lesion Cerebral palsy
a b s t r a c t To examine the development of basic finger–hand motor capacity in a one-year follow-up experiment performed on young children with bilateral spastic cerebral palsy (CP). The maximal finger grip strength (FGMAX), the frequencies of the fastest voluntary isometric finger force changes (FGCHANGE) while holding an object, in addition to the finger (FTAP) and hand tapping frequencies (HTAP) were examined on two separate occasions in 30 children between the ages of three to six years with bilateral spastic CP (BCSP). The examinations were performed 12 months apart in order to test for improvements in the aforementioned functions. After a one-year period of time, the FGMAX, FGCHANGE and FTAP values increased by 10–15% in both hands (changes in FTAP values were not statistically significant), while the HTAP values remained unchanged. In regard to the normative samples obtained from children of this age period, the gap in the motor capacity of the fingers did not increase. We observed an improvement in the basic finger functions over a one-year period of time in preschool aged children diagnosed with spastic CP. Interestingly, the improvement proceeded at a similar rate to that observed in normally developing children. However, the fastest hand tapping movements (HTAP) did not improve during this one-year time interval. In addition, we observed that in young children with BSCP, there appears to be considerable potential for the development and reorganisation of the elementary finger functions that are requisite for object manipulation. © 2009 Elsevier Ireland Ltd. All rights reserved.
The development of the fastest repetitive voluntary motor activity as assessed for different types of movements including fastest repetitive tapping movements, aiming movements and a pegboard transportation task has been shown to accurately reflect the maturation of the fastest cortico-motoneuronal efferents [11]. Furthermore, the development of central conduction times has been thought to influence the speed of repetitive movements in children. However, it has been observed that no significant improvements in the speed of these movements occurred when these movements were trained over a period of two consecutive days [11]. The development of fastest voluntary movements was therefore interpreted as a structure-bound phenomenon that was independent from learning. If this hypothesis is true, then children who are subjected to lesions in the cortico-motoneuronal efferents should demonstrate a massive slowing of the fastest voluntary movement. In children, the most common movement disorder, which also serves as one of the best “human models” to examine the role of early acquired lesions of the corticospinal
∗ Corresponding author. Tel.: +49 7043 16171; fax: +49 89 71009148. E-mail address: [email protected] (R. Blank). 0304-3940/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2009.03.058
pathways and their reorganisation, is a disorder known as bilateral spastic cerebral palsy (BSCP). Most children with BSCP have a periventricular lesion in the corticospinal pathways that had been acquired during the third trimester of pregnancy (the so-called “periventricular leucomalacia”). Some children have inherited malformations of the brain. The extent of damage caused by the lesion appears to be correlated with the functional severity of the disorder [15]. Since the corticospinal tract is particularly important for hand motor functions, the careful examination of the finger–hand motor capacity is of significant interest. Indeed, children with BSCP demonstrate a massive slowing of their fastest grip force changes and low grip strength [3]. The important issue of whether or not this reduction in motor capacity is stable over time remains unresolved; however, this issue is important since the lesion usually occurs during the third trimester of pregnancy. In a 13-year follow-up study, the grip-lift synergy was recorded in children with BSCP during the task of lifting an object [8]. The children in this study, who were between the ages of 6 and 8 years old, showed considerable improvement, with some individuals demonstrating a normalization of the grip-lift synergy values in comparison to normal experimental subjects after the long-term
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follow-up study. These results indicated that object manipulation can be improved without specific training over a long period of time. In addition, Duff and Gordon showed that even short-term repetitive training may improve the grip-lift synergy values [7]. However, grip-lift synergy is not only dependent on basic motor capacity but is also dependent on neuro-cognitive (such as the use of visual cues) and coordinative functions (such as the parallel programming of distal and proximal muscles of the upper extremities). From these studies, the question arises as to whether or not the grip-lift synergy has improved due to “unspecific” motor learning that occurs each day in an individual’s life or develops as a consequence of the maturation or reorganisation of the fastest cortico-motoneuronal efferents. Blank et al. showed that an intensive training period involving activities inherent to daily living may indeed change coordinative hand functions such as the grip-lift synergy but does not change basic motor capacity, such as the maximum tapping frequency or grip strength [5], which is in accordance with the observations reported by Muller and Homberg in normally developing children. This indicates that the impairment of basic motor capacity such as weakness (reduced grip strength) and spasticity (impaired ability in rapid movements or in grip force changes) is typical for corticospinal damage whereas lifting requires additional coordinative abilities and motor programming, which may be learned by performing everyday activities or by the implementation of training periods over time [7,17]. In addition, it is known that the gross motor function of cerebral palsy patients (GMFCS levels I–III) about 80–90% of the children reach their highest level of gross motor function between 5 and 7 years of age [6,13,18]. Therefore it is unknown whether or not there is any improvement or deterioration in the basic finger–hand functions in children with CP. Knowledge of such information may influence the potential for changes in function and activities over time. The motor capacity of the finger–hand functions is considerably improved in preschool-aged children. The most manipulative skills relevant to activities necessary for daily life appear to be acquired the same way in normally developed children as they are in children with cerebral palsy, during their respective life spans. Thus, it is of particular interest to understand if and how children of this age group who have been diagnosed with BSCP can alter their basic force and movement functions. The objective of the present longitudinal study was to examine the development of elementary finger and hand functions, including the finger (FTAP) and hand tapping (HTAP) values, the fastest isometric finger grip force changes (FGCHANGE) and the maximum grip strength (FGMAX) in children between the ages of three to six years old with spastic CP. The specific experiments involved the determination of whether there were general improvements or impairments in the basic motor capacity values of individuals over time, and whether these changes were different in CP children compared to normally developing children of the same age-group. These variables should be examined after a one year period without “specific” training, which means without the implementation of training sessions for tapping, grip strength and isometric force changes in the absence of medical treatment, since, for example, botulinum toxin is one drug known to influence these motor functions. We examined the longitudinal change in the following basic finger–hand functions: 1. The FGMAX and FGCHANGE values were measured in order to evaluate basic finger force functions. The forces were measured using an instrumented object (height × depth × width of 90 mm × 40 mm × 30 mm, weighing 200 g) containing a uniaxial force sensor that measured the grip force (0–100 ± 0.2 N)
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Fig. 1. The target variables of the fastest isometric force changes (frequency [Hz] = 1000/(duration of force increase + force decrease [ms])).
exerted against the grasping surface.1 The instrument was held using a hand precision grip with the thumb and digits 2 through 5 in an appropriate opposition. 2. The FTAP and HTAP values were determined to analyse the fastest finger and hand movements. For this set of experiments, a 3D movement analysis system (ultrasound based) was implemented.2 This analysis involved the use of an active marker system with small markers on the hand that transmit ultrasound waves to a receiver. Upon receiving the signals, the markers could easily be analysed and the temporo-spatial variables could then be calculated. The markers were placed on the nail of the index finger, over the joint between the index finger and the hand, and over the joint of the wrist of the hand (middle). The patients performed the standardized tasks using their preferred and their non-preferred hands separately. Hand preference was determined by observation of activities inherent to daily living (modified to Salmaso and Longoni [14]. In addition, the children were instructed to perform the following tasks: 1. In the FGMAX experiments, the children were instructed to press the box as often as possible (“squeeze out like an orange”). The children had at least 3 trials, with each trial lasting 20 s, in order to ensure understanding of the experimental parameters and in order to prevent fatigue. Within this observation period, the maximum grip force (best performance) was used for analysis. 2. In the FGCHANGE experiments the children were instructed to increase and decrease (press and release) their grip force while holding the box as often as they could within a time period of 20 s. In order to ensure that the children understood the task, the children could see their actual grip force increasing and decreasing on a computer screen (no tracking of a visual cue was used and the target variables are displayed in Fig. 1). 3. In the FTAP experiment, the children were instructed to tap on a table using their index finger as quickly as possible. In this set of experiments, the target variable was the tapping frequency. The dimension of the measurement was the number of movements per second.
1 Manufacturer: Research Group Clinical Neuropsychology, Clinical Center of Bogenhausen, Munich, Germany. 2 Zebris Medical GmbH, Max-Eyth-Weg 42, D-88316 Isny im Allgäu, E-mail: [email protected].
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4. In the HTAP experiments, the children were instructed to tap on the table with their hand as quickly as possible. In this set of experiments, the target variable was the tapping frequency. The dimension of the measurement was the number of movements per second. In order to ensure that the children understood the experimental setup and in order to minimize the training effects, the children were instructed to practice each test. In order to minimize the effects of fatigue and motivation, only the fastest five periods were used for statistical analysis in tasks two to four. Since we used only short test periods and evaluated only the best performance from each child, the results are not likely to be influenced by fatigue. Overall, a total population of 30 children, which consisted of 22 boys and 8 girls (5 three-year olds, 11 four-year olds, 12 fiveyear olds, 2 six-year olds) and included 20 children preferred using their right hands and 10 children preferred using their left hands in activities of daily living (e.g. playing, eating). All of these children were diagnosed with BSCP according to the criteria established by the Surveillance of Cerebral Palsy in Europe (SCPE) and were examined two separate times, with a period of 12 months between each examination [1]. Hand laterality was assessed by the observation of activities inherent to daily living that could be performed by each child. The severity of each test was classified according to the Manual Ability Classification System (MACS) [9] that included the following criteria (three levels of severity): I. The ability to handle objects easily and successfully. At most, there may be limitations in the ease of performing manual tasks that require speed and accuracy. However, any limitations in these manual abilities do not restrict the independence of performing daily activities. II. The ability to handle most objects with somewhat reduced quality and/or speed of achievement. Here, certain activities may be avoided or may be performed with some difficulty. In addition, alternative ways of performing a task may be used but manual abilities do not usually restrict the independence of performing daily activities. III. The ability to handle objects with difficulty. Here, children need help preparing and/or modifying activities. Their performance is slow and achieved with limited success in regard to the quality and quantity of the performance. The activities could be performed independently if they were previously arranged or had been adapted. The MACS levels were distributed among level I 8, level II 11, and level III 11. During the one-year period of the experiment, the children received no therapy aiming to improve basic motor capacities such as strengthening or anti-spastic treatments. This could be controlled as all children would have needed prescriptions by medical doctors for such therapies. The quality and quantity of general interventions were equivalent to those being described in detail in Blank et al. [5]. The children repetitively practiced everyday activities within a Conductive Education program (three blocks of four weeks) and further low intensity standard programs that were typical for children of this age group. In this previous study, even the high-intensity intervention has failed to show any effects on basic motor activities like FGMAX, FGCHANGE, FTAP and HTAP [5]. Furthermore, we examined the changes in the relationship between normally developing children and children with BSCP of the same age, in order to predict whether or not the differences in the measured variables between children with BSCP and normally developing children increases or decreases. Thus, we performed an age-normalised comparison with a reference sample of
normally developing children. These data were transformed into age-corrected values (“z-values”), which were based on a sample of 125 normally developing children between the ages of three and six years old with no history of therapy, no neurological abnormalities, and no deficits in everyday function. Neurological impairments, especially fine motor problems were excluded by history and by clinical examination according to Touwen [16]. These normally developing children were gathered from two kindergarten classrooms and served as standardization samples. The z-values for the children with BSCP were calculated using the individual value of the child with BSCP minus the mean standard value determined from the children of the corresponding healthy age group. This was then divided by the standard deviation of the mean value of the healthy corresponding age-group. For example, a z-value of +2.1 indicates that the child had a value that was 2.1 standard deviations above the mean of a normal child from the same age, thus indicating greater than 2 standard deviations, or in other words, a value that is above 97.5% of the reference sample of the same age. On the other hand, a z-value of −2.3 indicates that the child had a value that was 2.3 standard deviations below the average value obtained from a normal child of the same age, thus indicating greater than 2 standard deviations below the mean of a normally developed child of the same age (below 2.5% of the reference sample). The follow-up examination, which occurred 12 months later, was evaluated using t-tests for dependent samples (each child served as own control that means data of the first and second tests were dependent from each other). In a second analysis, all children that could not be examined on both occasions or dropped out in one test because of specific difficulties (e.g. finger tapping appeared to be more difficult than maximum grip force) received the same values as their other examination (effect was set as zero effect). Children that could not perform a test twice receive the mean value of all other children during the first examination at both examinations (again effect was set to zero). The examination was performed within a playful setting and within the usual diagnostic setting. The ethical principles outlined in the Declaration of Helsinki were followed. For statistical analysis, the Statistical Package SPSS, Version 12.0 was used.3 Data before and after 12 months were obtained from 28 children for FGMAX, from 27 children FGCHANGE, from 26 children for FTAP, and from 21 children for HTAP (preferred hands). The significant decrease in the number of children analysed via the HTAP test was a consequence of the fact that six children (n = 1 for MACS level I, n = 1 for MACS level II, and n = 4 for MACS level III) during the first examination, and four children one year later (n = 1 for MACS I, n = 2 for MACS II, and n = 1 for MACS III) were not able to perform the task according to the instructions. In regard to the use of the non-preferred hands, the drop-out rate was much higher. After completing both examinations, data could only be analysed for 13 children in the FGMAX analysis, for 9 children in the FGCHANGE analysis, for 5 children in the FTAP analysis, and for 7 children in the HTAP analysis. Thus, the results of the non-preferred hands cannot be interpreted due to a lack of sufficient data. Nevertheless, the drop-out analysis showed that drop-out rates were higher for the first examination than for the second examination that suggested some improvement in these motor skills (drop-outs of the first examination versus the second examination include n = 10 for the FGMAX first examination versus n = 9 for the second examination, n = 16 for the FGCHANGE first examination versus n = 11 for the second examination, n = 24 for the FTAP first examination versus n = 9 for the second examination,
3
IL.
SPSS Inc. Headquarters, Corporate Headquarters, 233 S Wacker Drive, Chicago,
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and n = 22 for the HTAP first examination versus n = 9 for the second examination). Within one year, the values of the FGMAX analysis improved considerably from (means) 27.8N (SD 11.4) to 34.5 N (SD 11.6) (t = −3.4, p < 0.001) for the preferred hands and from 23.8N (SD 7.0) to 26.9 N (SD 8.5) (t = (2.7, p < 0.001) for the non-preferred hands (Fig. 2). The values for the FGCHANGE analysis also improved significantly for the preferred hands, increasing by approximately 15% from the mean value of 1.5 Hz (SD 0.60) to 1.8 Hz (SD 0.57) of force change per sec (t = 3.9, p < 0.001). In regard to the non-preferred hands, there was an improvement of approximately 10% (1.30 Hz (SD 0.46) to 1.43 Hz (SD 0.38)) but these values were not statistically significant due to the small number of children being able to perform the test using their non-preferred hands (Fig. 2). In addition, the values for the FTAP analysis improved by roughly 10% (mean frequency and standard deviation (SD) values for the preferred hand increased from 1.73 Hz (0.55) to a value of 1.91 Hz (0.43) while these values also increased for the non-preferred hand from 1.77 Hz (0.51) to 1.86 Hz (0.60)). However, due to the variability of the group sizes, the changes were not statistically significant. Interestingly, the values for the HTAP analysis did not show a statistically significant increase (the mean values (SD) for the frequencies of the preferred hand increased from 1.97 Hz (0.58) to 1.98 Hz (0.52) while the mean values for the non-preferred hand increased from 1.48 Hz (0.75) to 1.56 Hz (0.58), which was not significant here). If the drop-outs were included by setting their effects to zero the results were as follows (preferred hands): FGMAX: T0 29.69N (SD 9.81), T12 34.36N (SD 9.81), t = 3.7, p < 0.001, FGCHANGE: T0 1.59 (SD 0.49), T12 1.9 (SD 0.51), t = 4.2, p < 0.001, FTAP: T0 1.73 (SD 0.59), T12 1.86 (SD 0.50), t = 1.3, n.s., HTAP: T0 1.85 (SD 0.47), T12 1.94 (SD 0.47), t = 1.2, n.s. This means all basic motor functions improved; however, finger and hand tapping became not significant because of higher variation and slightly lower mean changes. Because of high drop-outs and high variation of the data the results on the non-preferred hands can only be interpreted in a descriptive way e.g. by comparing the drop-out rates on both exam-
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inations. A quantitative analysis by alluding missing data to zero effect seemed to be not sensitive. When these results are transferred to the age-related changes observed in normally developing children, the improvement in the force parameters indicated that the gap between normal children and children with CP decreased slightly, however this decrease was not statistically significant (Fig. 3). This indicates that the age-related changes in both normally developing children and in children with CP were similar. In regard to the finger movement velocities, the gap between normally developing children and children with CP remained approximately equivalent (Fig. 3). These results indicated that the changes related to age were similar upon comparison to normally developing children. Thus, within a time period of one year, the elementary motor functions of the fingers of preschool children with BSCP improved by 10–15%. This rate of change is similar to the rate of change observed in normally developing children. This increase is relevant since these changes are the basis for relevant improvements in the activities inherent to daily living as observed in preschool children. In addition, we conclude that the HTAP values did not change over the one-year period of time analysed in this study. Longitudinal changes in the capacity of basic finger and hand motor skills were examined in children between the ages of three and six years olds. Hand tapping was most difficult task for the children to perform since it dealt with the hand and not with the entire arm. The drop-out analysis shows that drop-outs are less common in the second set of examinations. This is consistent with our observation of general improvement. Further, “zero-correction” of missing data did not change the general results. Therefore, concerning the results on the preferred hands we are quite confident that the drop-outs do not influence the general results. The results on the non-preferred hands also indicate improvements but cannot be interpreted quantitatively in comparison with the preferred hands because of a high proportion of drop-outs. The results presented herein indicate that the relevant development of fine motor functions is usually observed within a one-year period in this age group. It is important to point out that the lesions or malformations of the corticospinal tract that resulted in children having BSCP had likely occurred during the third trimester of pregnancy.
Fig. 2. The development of maximum grip force and fastest isometric force changes in children between the ages of 3–6 years old with bilateral spastic cerebral palsy within one year (preferred and non-preferred hands) where T0 = first examination, T12 = second examination after 12 months; **p < 0.01, *p < 0.05, ◦ p = 0.06.
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Fig. 3. The age-corrected comparison of the development of the elementary finger–hand functions (maximum grip force, fastest isometric force changes, finger and hand tapping frequency) in children between the ages of 3–6 years old with bilateral spastic cerebral palsy within one year as compared to the development of a normal children of the same age (mean ± standard deviation is z = 0 ± 1 based on a population of 125 normal children), where T0 = first examination, T12 = second examination after 12 months, and n.s. = not significant).
A major unresolved issue involves whether or not these improvements in motor functions over time are caused by structural changes of the moto-neurocortical network (such as “maturation,” which is an intrinsic effect) or by therapeutic interventions (such as “environmental effects”, which are extrinsic effects). For ethical reasons, therapeutic intervention was required over a significantly long time interval. We cannot completely exclude the possibility that environmental (therapeutic) factors interfered with these results. This situation invokes a kind of nature-nurture problem. However, we believe that there is some evidence from previous studies indicating that intrinsic effects may mainly be responsible for such observations. Muller and Homberg have previously shown that the development of basic motor capacity in normally developing children is related to structural changes that occur in the moto-corticospinal efferents [11]. An intensive training period involving elementary finger–hand functions, such as tapping, performed on two consecutive days did not show any significant improvement. In addition, Duff et al. have shown that in contrast to basic motor capacity such as lifting an object, a coordinative function can be improved in children with CP within a short period of time that involves repetitive training.
In addition, a study by Blank et al. supports both of the aforementioned findings [5]. Indeed, Blank et al. have shown in an A–B–A study that within a nine-month period involving intensive training activities inherent to daily living (7 h a day), it is possible to improve coordinative functions such as lifting (as reported by Eliasson), but there was no additional effect of intensive therapy on basic finger–hand functions (tapping, grip strength, etc.) when compared to phases without intensive training. As the children in the present study received equivalent therapeutic input to the previous study [5] we can assume that the changes of basic motor capacity over time are not caused by training effects. The data presented herein show that, in spite of the lesions to their moto-corticospinal efferents, children with BSCP can improve their finger grip strength, finger movement velocity and maximum isometric finger force rates by 10–15% within a one-year period. In addition, the similar rate of change over time also observed in normally developing children leads to the hypothesis that a certain amount of intact moto-neuronal efferents and networks may be responsible for these positive changes. The motor capacity of the fingers appears to improve particularly in this age group without specific strength training or training of the elementary finger–hand movement by invoking exercises such as tapping.
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On the basis of the studies mentioned, we believe that the significant improvements of coordinative functions such as lifting, as reported by Eliasson et al. after a 13-year period, should be interpreted by developmental effects on the basis of structural changes to the intact moto-neurocortical networks (intrinsic changes) in addition to training effects (extrinsic changes) [8]. The second finding of our study was that more proximal functions such as the velocity of wrist flexion and extension during hand tapping did not improve within this period of observation. However, one needs to be very careful with further interpretations because of the high drop-out rate in the hand tapping task. It seems that children with BSCP below six years of age have more potential to improve distal motor functions than more proximally generated movements. In addition, different developmental profiles for finger and hand movements have also been shown, for example, in the process of drawing with a pencil in normally developing children [4]. So far, there are no longitudinal studies focused on hand motor functions in children with CP that address the changes over time within and between certain severity levels classified by the MACS. For gross motor functions, high stability over time was found and even “gross motor function curves” could be established [12]. Beckung et al. and Hanna et al. showed that most children with spastic CP reached their “peak” performance between the 5th and 7th anniversary although there may be some variability between the gross motor development of children with CP [2,10]. This means that the differences in gross motor functions between normal developing children and children with CP steadily increase during kindergarten age. This is in accordance with early studies involving the walking prognosis of children with CP [6,13,18]. The present findings indicate that the prognosis of fine motor capacity may be better. The different development of the finger motor functions as compared to the proximal or gross motor functions may be explained by the nature of the periventricular lesions in children with CP. The corticospinal pathways to the fingers are more distant from the periventricular area than those to the lower extremities and therefore, they may be less affected by periventricular lesions in children with spastic cerebral palsy. On the other hand, the input of cortico-motoneuronal efferents that control the finger function is particularly important and it is likely that a number of efferents may still be intact in order to procure the normal pattern of development, but the number of intact efferents may not be sufficient to achieve normal finger strength and velocity. The results of this study may thus have important therapeutic implications. The specific improvement of the basic finger motor functions in children with BSCP may suggest that there may be potential for intensive therapeutic approaches in specifically improving finger–hand functions, as opposed to gross motor functions. In conclusion, this study supports the hypothesis that in young children with BSCP, the basic motor capacity of the finger functions considerably improves during preschool years in spite of the
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presence of the lesions. Studies examining the long-term effects of therapeutic interventions on finger–hand functions in children of this age should take into consideration these changes over time. Acknowledgement We wish to thank to the clinical and laboratory staff of the Department of Sensomotor Functions of the Child Centre Munich that supported the examination of the children within the clinical setting. References [1] Surveillance of cerebral palsy in Europe: a collaboration of cerebral palsy surveys and registers. Surveillance of Cerebral Palsy in Europe (SCPE), Dev. Med. Child Neurol. 42 (2000) 816–824. [2] E. Beckung, G. Carlsson, S. Carlsdotter, P. Uvebrant, The natural history of gross motor development in children with cerebral palsy aged 1 to 15 years, Dev. Med. Child Neurol. 49 (2007) 751–756. [3] R. Blank, J. Hermsdorfer, Basic motor capacity in relation to object manipulation and general manual ability in young children with spastic cerebral palsy, Neurosci. Lett. 450 (2009) 65–69. [4] R. Blank, V. Miller, H. von Voss, R. von Kries, Effects of age on distally and proximally generated drawing movements: a kinematic analysis of school children and adults, Dev. Med. Child Neurol. 41 (1999) 592–596. [5] R. Blank, R. von Kries, S. Hesse, H. von Voss, Conductive education for children with cerebral palsy: effects on hand motor functions relevant to activities of daily living, Arch. Phys. Med. Rehabil. 89 (2008) 251–259. [6] A.C. Da Paz junior, S.M. Burnett, L.W. Braga, Walking prognosis in cerebral palsy: a 22-year retrospective analysis, Dev. Med. Child Neurol. 36 (1994) 130–134. [7] S.V. Duff, A.M. Gordon, Learning of grasp control in children with hemiplegic cerebral palsy, Dev. Med. Child Neurol. 45 (2003) 746–757. [8] A.C. Eliasson, H. Forssberg, Y.C. Hung, A.M. Gordon, Development of hand function and precision grip control in individuals with cerebral palsy: a 13-year follow-up study, Pediatrics 118 (2006) e1226–e1236. [9] A.C. Eliasson, L. Krumlinde-Sundholm, B. Rosblad, E. Beckung, M. Arner, A.M. Ohrvall, P. Rosenbaum, The Manual Ability Classification System (MACS) for children with cerebral palsy: scale development and evidence of validity and reliability, Dev. Med. Child Neurol. 48 (2006) 549–554. [10] S.E. Hanna, P.L. Rosenbaum, D.J. Bartlett, R.J. Palisano, S.D. Walter, L. Avery, D.J. Russell, Stability and decline in gross motor function among children and youth with cerebral palsy aged 2 to 21 years, Dev. Med. Child Neurol. (2009), doi:DMCN3196 [pii] 10.1111/j.1469-8749.2008.03196.x. [11] K. Muller, V. Homberg, Development of speed of repetitive movements in children is determined by structural changes in corticospinal efferents, Neurosci. Lett. 144 (1992) 57–60. [12] R.J. Palisano, D. Cameron, P.L. Rosenbaum, S.D. Walter, D. Russell, Stability of the gross motor function classification system, Dev. Med. Child Neurol. 48 (2006) 424–428. [13] A. Sala, D. Grant, Prognosis for ambulation in cerebral palsy, Dev. Med. Child Neurol. 37 (1995) 1020–1026. [14] D. Salmaso, A.M. Longoni, Problems in the assessment of hand preference, Cortex 21 (1985) 533–549. [15] A. Soot, T. Tomberg, P. Kool, R. Rein, T. Talvik, Magnetic resonance imaging in children with bilateral spastic forms of cerebral palsy, Pediatr. Neurol. 38 (2008) 321–328. [16] B. Touwen, The Neurological Examination of the Child with Minor Nervous Dysfunction, Georg-Thieme Verlag, Stuttgart, New York, 1982. [17] D.V. Vaz, M. Cotta Mancini, S.T. Fonseca, D.S. Vieira, A.E. de Melo Pertence, Muscle stiffness and strength and their relation to hand function in children with hemiplegic cerebral palsy, Dev. Med. Child Neurol. 48 (2006) 728–733. [18] E. Wood, P. Rosenbaum, The gross motor function classification system for cerebral palsy: a study of reliability and stability over time, Dev. Med. Child Neurol. 42 (2000) 292–296.