Research in Developmental Disabilities 35 (2014) 3574–3581
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Research in Developmental Disabilities
Individuals with intellectual disability have lower voluntary muscle activation level Rihab Borji a,*, Firas Zghal b, Nidhal Zarrouk c, Sonia Sahli a, Haithem Rebai a a
Unite´ de Recherche Education, Motricite´, Sports et sante´, Institut Supe´rieur du Sport et de l’Education Physique de Sfax, Universite´ de Sfax, Tunisia b Laboratoire Adaptations Me´taboliques a` l’Exercice en Conditions Physiologiques et Pathologiques (AME2P, EA 3533), Universite´ Blaise Pascal, Clermont-Ferrand, France c Laboratoire des techniques d’imagerie me´dicale (LR 12ES06, LTIM), Faculte´ de Me´dicine de Monastir, Universite´ de Monastir, Tunisia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 6 June 2014 Received in revised form 26 August 2014 Accepted 28 August 2014 Available online 20 September 2014
The aim of this study was to explore the voluntary activation level during maximal voluntary contraction (MVC) in individuals with intellectual disability (ID) versus individuals without ID using the twitch interpolation technique. Ten individuals with mild ID (ID group) and 10 sedentary men without ID (control group) participated in this study. The evaluation of neuromuscular function consisted in three brief MVCs (3 s) of the knee extension superimposed with electrical nerve stimulation (NES) to measure voluntary activation. Muscle activity levels were also measured with surface EMG. The root mean square (RMS) was extracted from the EMG signal. The RMS/Mmax ratio and the neuromuscular efficiency (NME) were calculated. Our results reported that individuals with ID present lower muscle strength (p < 0.001), lower voluntary activation level (p < 0.001), lower RMS values of vastus lateralis (p < 0.05), vastus medialis (p < 0.05), and rectus femoris (p < 0.001) muscles. In addition, our results showed lower RMS/Mmax values in the ID group than in the control group for the VM (0.05 0.01 mV vs. 0.04 0.01 mV; p < 0.05) and the RF (0.06 0.02 mV vs. 0.05 0.02 mV; p < 0.05) muscles. However, no significant difference was reported for the VL muscle (0.05 0.02 mV vs. 0.05 0.02 mV; p = 0.463). Moreover, Individuals with ID present smaller potentiated twitch (p < 0.001). However, no significant difference was reported in the NME ratio. These results suggest that the lower muscle strength known in individuals with ID is related to a central nervous system failure to activate motor units and to some abnormal intrinsic muscle properties. It seems that the inactive lifestyle adopted by individuals with ID is one of the most important factors of their lower voluntary activation levels. Therefore, physical activities should be introduced in life style of individuals with ID to improve their neuromuscular function. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Intellectual disability Electrical stimulation Twitch interpolation technique Voluntary activation level Knee extensor muscles
1. Introduction Individuals with intellectual disabilities (ID) present several abnormalities in their nervous system structure (Gabrielli et al., 1998) localized in the white matter tracts that are responsible for the processing of sensory and motor
* Corresponding author at: Institut Supe´rieur de Sport et de l’Education Physique de Sfax, Route de l’Ae´rodroˆme, Km 3.5, BP 1068, 3000 Sfax, Tunisia. Tel.: +216 22092322. E-mail addresses: [email protected] (R. Borji), zghal.fi[email protected] (F. Zghal), [email protected] (N. Zarrouk), [email protected] (S. Sahli), [email protected] (H. Rebai). http://dx.doi.org/10.1016/j.ridd.2014.08.038 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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information (Yu et al., 2008). Several studies have mentioned that individuals with ID present several abnormalities in motor nervous control and neuromuscular coordination (Chia, Lee, & Teo-Koh, 2002). In addition, individuals with ID present lower muscle strength compared to individuals without ID (Angelopoulou, Tsimaras, Christoulas, Kokaridas, & Mandroukas, 1999; Blomqvist, Olsson, Wallin, Wester, & Rehn, 2013; Borji, Sahli, Zarrouk, Zghal, & Rebai, 2013; Carmeli, Ayalon, Barchad, Sheklow, & Reznick, 2002; Horvat, Croce, Pitetti, & Fernhall, 1999). Moreover, in a previous study, we demonstrated that individuals with ID present lower root mean square (RMS) value in comparison with individuals without ID (Borji et al., 2013). Nevertheless, the reason for this force deficiency has not been identified yet. In individuals without ID, it has been demonstrated that muscle force level depends on several factors such as muscular fiber typology (Fitts & Widrick, 1996), training status (Fitts & Widrick, 1996), sex difference (Miller, MacDougall, Tarnopolsky, & Sale, 1993), and age difference (Lindle et al., 1997). Muscle force level depends also on neural mechanisms such as the voluntary activation level of motor units (Gandevia, 2001, 1992). Voluntary activation describes the level of neural drive of muscle during voluntary contractions (Gandevia, Allen, & McKenzie, 1995). One of the methods to evaluate the activation of motor units by the central nervous system is the superimposed twitch technique (Gandevia, 2001; Millet et al., 2012). The presence of a superimposed twitch produced by motor nerve stimulation during a MVC indicates that the whole motor units are not totally recruited by the central nervous system (Merton, 1954). If voluntary activation is incomplete, failure to drive the muscle should occur at or above the site of stimulation of the motor axons (Merton, 1954). Using this technique, many studies have attempted to investigate the relationship between the reduced voluntary force production and the voluntary activation levels in general population (Belanger & McComas, 1981; Bigland-Ritchie, Donovan, & Roussos, 1981), athletic population (Huber, Suter, & Herzog, 1998), and clinical populations (Hurley, Jones, & Newham, 1994; Rutherford, Jones, & Newham, 1986). Studies investigating this relationship in elderly persons and individuals with cerebral palsy found that the lower muscle force noted in both populations had been related to the activation deficit (AD) from central nervous system (Stackhouse et al., 2001; Stackhouse, Binder-Macleod, & Lee, 2005; Yue, Ranganathan, Siemionow, Liu, & Sahgal, 1999). Nevertheless, to our knowledge no data is available about the voluntary activation in individuals with ID. Thus, the aims of this study were to compare the force production and the level of voluntary activation between individuals with ID and individuals without ID as well as to investigate the implication of the central nervous system deficiency in the force production in individuals with ID. 2. Methods 2.1. Participants The sample population consisted of 20 sedentary men who met the same criteria in terms of socioeconomic status and ethnicity. Ten men with ID (age = 24.9 4.9 years; height = 1.7 0.1 m; weight = 77.9 8.3 kg; BMI = 25.7 2.5 kg/m2) participated in the study as an experimental group. The control group consisted of 10 sedentary and healthy (no cardiovascular, metabolic, immunologic, or neuromuscular disorders) men without ID matched for age, height, and weight: (age = 25.2 2.7 years; height = 1.7 0.1 m; weight = 75.3 9.2 kg; BMI = 23.9 1.7 kg/m2). All participants with ID suffered from a mild ID with an intelligence quotient (IQ) between 50 and 55 and 70 (The American Psychiatric Association, 2000) determined by the WAIS-IV test (Wechsler, 2008) elaborated by the educational center psychologist (IQ = 62 3.5). Participants with ID have been recruited randomly from the Tunisian Union of Aid to Mental Insufficiency (TUAMI). The sample excluded individuals with down syndrome, and with multiple disabilities. The participant’s morphological characteristics showed no statistical differences in terms of age, weight, height and BMI between the two groups. The participants were fully informed of the procedure and the risks involved and gave their written consent. The informed consent for the individuals with ID was provided by their parents or legal guardians. 2.2. Study design Three days after a familiarization session with the experimental procedures, participants engaged in the experimental session. The experimental session was preceded by a warm-up consisting of several submaximal contractions (12–15) of knee extension muscles at a freely chosen intensity. The evaluation of neuromuscular function consisted in three brief (3 s) maximal voluntary contractions (MVCs) of the knee extension superimposed with nerve electrical stimulation (NES) to measure voluntary activation. Muscle activity levels were also measured with surface electromyography (EMG). To exclude the confounding effect of fatigue induced by repeated muscular contractions, the three MVCs were separated by a 2-min recovery period. The comparison of data obtained during the first and the third MVC did not reveal any significant difference, suggesting that the experimental procedures did not induce any fatigue. 2.3. Testing procedures and instrumentation 2.3.1. Force measurement The participants performed three MVCs with strong encouragement by the investigator. During testing, the participants were seated on an isometric dynamometer (Good Strength, Metitur, Finland) equipped with a cuff attached to a strain gauge. This cuff was adjusted 2 cm above the lateral malleolus using a Velcro strap. The participants stabilized themselves by
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grasping handles on the side of the chair during contractions. Safety belts were strapped across the chest, thighs and hips to avoid lateral, vertical or frontal displacements. All measurements were taken from the participant’s dominant leg, with the hip and knee angles set at 908 from full extension (= 08). All participants in our study presented the right leg as the dominant leg (determined by the leg used to kick a ball). 2.3.2. Electromyographic recordings The EMG signals of the vastus lateralis (VL), vastus medialis (VM) and rectus femoris (RF) muscles were recorded using bipolar silver chloride surface electrodes (Blue Sensor N-00-S, Ambu, Denmark) during MVC and stimulations. The recording electrodes were taped lengthwise on the skin over the muscle belly following SENIAM recommendations (Hermens, Feriks, Disselhorst-Klug, & Rau, 2000), with an inter-electrode distance of 20 mm. The position of the electrodes was marked on the skin in case they needed to be repositioned during the experiment. The reference electrode was attached to the patella. Low impedance (Z < 5 kV) at the skin-electrode surface was obtained by shaving, abrading the skin with thin sand paper and cleaning with alcohol. EMG signals were amplified (Octal Bio Amp ML 138, ADInstruments, Australia) with a bandwidth frequency ranging from 10 Hz to 1 kHz (common mode rejection ratio > 96 dB, gain = 1000) and simultaneously digitized together with the force signals using an acquisition card (Powerlab 16SP, ADInstruments, Australia) and Labchart 7.0 software (ADInstruments, Australia). The sampling frequency was 2 kHz. MVC force was determined as the peak force reached during maximal efforts. RMS values of the VL, VM and RF EMG activities were calculated during the MVC trials over a 0.5 s period after the force had reached a plateau and before the superimposed stimulation was evoked. Neuromuscular efficiency (NME) was calculated as the ratio of peak force to the sum RMS of the VL, RF, and VM muscles to provide an overall representation of quadriceps muscle group activity (Deschenes et al., 2002; Woods & Bigland-Ritchie, 1983; Zarrouk et al., 2012). 2.3.3. Peripheral nerve stimulation (NES) The twitch interpolation method, proposed by Merton (1954), involves interpolation of a single supramaximal electrical stimulus to the motor nerve during MVC. Voluntary activation is thus quantified by comparing the amplitude of the superimposed twitch with the force evoked by the same stimulus intensity at rest, and immediately following the corresponding MVC (Kufel, Pineda, & Mador, 2002). The femoral nerve was stimulated percutaneously with a single squarewave stimulus of 1 ms duration with maximal voltage of 400 V delivered by a constant current stimulator (Digitimer DS7A, Hertfordshire, United Kingdom). The cathode (self-adhesive electrode: Ag–AgCl, 10 mm diameter) was positioned in the femoral triangle and pressed firmly into place by an experimenter. The anode, a 10 5 cm self-adhesive stimulation electrode (Medicompex SA, Ecublens, Switzerland) was placed midway between the greater trochanter and the iliac crest. Optimal stimulation intensity was determined from M-wave and force measurements before each testing session. Briefly, the stimulation intensity was increased by 5 mA until there was no further increase in either peak twitch force (i.e., the highest value of the knee extension twitch force was reached) or in concomitant VL, VM and RF peak-to-peak M-wave amplitudes (Mmax). During the subsequent testing procedures, the intensity was set to 150% of the optimal intensity to overcome the potential confounding effect of axonal hyperpolarization (Burke, 2002). MVC superimposed with NES were used to calculate the voluntary activation level as follows: 1 superimposed twitch Voluntary activation ð%Þ ¼ 100 potentiated twitch where ‘‘superimposed twitch’’ is the amplitude of the twitch evoked with NES during MVC and ‘‘potentiated twitch’’ is the amplitude of the twitch evoked by a single stimulation delivered 3 s after the end of the MVC. This provided the opportunity to obtain a potentiated mechanical response and so reduce the variability in voluntary activation values (Kufel et al., 2002). The ID group AV was calculated as follows: 1 voluntary activation of ID group AV ð%Þ ¼ 100 voluntary activation of control group 2.4. Statistical analysis All data are presented as means SD and were analyzed by the Statistica for Windows software (version 6.0, StatSoft, Inc., Tulsa, OK). Data distribution normality was confirmed with the Shapiro–Wilk W-test. Independent sample t-tests were executed in order to analyze group differences in characteristics (age, height, weight and BMI), MVC, voluntary activation, potentiated resting twitch, RMS, RMS/Mmax and NME values. The level of significance for all statistical analyses was set at p < 0.05. 3. Results 3.1. Mechanical responses The independent sample t-test demonstrated a significant (p < 0.001) difference in MVC between ID group and control group. Individuals with ID demonstrated lower maximal force producing capacity (439.6 62.7 N vs. 704.1 125.4 N; Fig. 1).
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900 800 700
MVC (N)
600 500 400 300 200 100 0
Controls
ID
Fig. 1. Mean ( SD) values of maximal voluntary contraction (MVC) for individuals with intellectual disability (ID) and those without ID (controls). *** Significant difference at p < 0.001.
Voluntary Activation Level NES (%)
100 90 80 70 60 50 40 30 20 10 0
Contrrols
ID
Fig. 2. Mean ( SD) values of voluntary activation level for individuals with intellectual disability (ID) and those without ID (controls). *** Significant difference at p < 0.001.
Potentiated Resting Twitch (N)
250 200 150 100 50 0
Contro ols
ID
Fig. 3. Mean ( SD) values of potentiated resting twitch (PRT) for individuals with intellectual disability (ID) and those without ID (controls). *** Significant difference at p < 0.001.
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Table 1 Root mean square (RMS), RMS/Mmax values of the vastus lateralis (VL), vastus medialis (VM), and rectus femoris (FR) muscles and neuromuscular efficiency (NME) ratio for individuals with intellectual disability (ID group) and those without ID (controls).
RMS VL (mV) RMS VM (mV) RMS RF (mV) RMS/Mmax VL (mV) RMS/Mmax VM (mV) RMS/Mmax RF (mV) NME
Control group (n = 10) Mean (SD)
ID group (n = 10) Mean (SD)
Independent t-tests (p-value)
0.42 (0.15) 0.51 (0.22) 0.47 (0.17) 0.05 (0.02) 0.05 (0.01) 0.06 (0.02) 536.8 (158.7)
0.27 (0.15) 0.29 (0.07) 0.29 (0.06) 0.05 (0.02) 0.04 (0.01) 0.05 (0.02) 539.3 (144.7)
2.13 2.79 3.02 0.74 2.59 2.55 0.03
(0.046)* (0.012)* (0.007)*** (0.463) (0.018)* (0.020)* (0.970)
* Significant differences at p < 0.05. *** Significant differences at p < 0.001.
In addition, the independent sample t-test indicated a significant (p < 0.001) differences for both voluntary activation and potentiated resting twitch between the ID group and the control group. Individuals with ID presented lower voluntary activation level (65.8 8.0% vs. 85.6 5.0%; Fig. 2) and potentiated resting twitch (115.8 18.9 N vs. 186.3 24.3 N; Fig. 3). 3.2. EMG responses The independent sample t-test indicated significantly lower RMS values in the ID group than the control group for the VL (0.27 0.15 mV vs. 0.42 0.15 mV; p < 0.05), the VM (0.29 0.07 mV vs. 0.51 0.22 mV; p < 0.05), and the RF (0.29 0.06 mV vs. 0.47 0.17 mV; p < 0.001) muscles. Moreover, the independent sample t-test indicated significantly lower RMS/Mmax values in the ID group than the control group for the VM (0.05 0.01 mV vs. 0.04 0.01 mV; p < 0.05) and the RF (0.06 0.02 mV vs. 0.05 0.02 mV; p < 0.05) muscles. However, no significant difference was reported for the VL muscle (0.05 0.02 mV vs. 0.05 0.02 mV; p = 0.463; Table 1). Concerning the NME ratio, the independent sample t-test indicated no significant difference between the ID group and the control group (539.3 144.7 vs.536.8 158.7; p = 0.97; Table 1). 4. Discussion The aims of this study were to compare the force production and the level of voluntary activation between individuals with ID and individuals without ID as well as to investigate the implication of the central nervous system deficiency in the force production in individuals with ID. Our results showed that individuals with ID develop lower MVC than individuals without ID. This result is consistent with previous studies investigating muscle force level in sedentary individuals with ID (Angelopoulou et al., 1999; Borji et al., 2013; Carmeli et al., 2002; Croce, Pitetti, Horvat, & Miller, 1996; Horvat et al., 1999; Pitetti & Boneh, 1995; Zafeiridis et al., 2010). Besides, smaller differences in force level were reported when comparing elite athletes with ID to physical education students without ID (van de Vliet et al., 2006). Moreover, it has been demonstrated that, in individuals without ID, the muscle force level depends on the training status (Fitts & Widrick, 1996) and the voluntary activation level (Gandevia, 2001, 1992). The main result of our study showed that individuals with ID have lower ability to activate motor units than individuals without ID. They were only able to activate 65% of their motor units versus 85% in the control group. Moreover, our ID group presents an AD of 23.13% compared with the control group. Even in individuals without ID, it is well known that the central nervous system fails to generate maximal evocable force (Gandevia, 2001; Strojnik, 1995). Therefore, concerning our control group, our results were in agreement with those of Shield and Zhou (2004) who found that the quadriceps voluntary activation was between 85% and 95% of total motor units in sedentary individuals without ID. Moreover, Babault, Pousson, Ballay, and Van Hoecke (2001) found that the mean activation levels during MVC are 95.2% in individuals practicing regular physical activities. Unfortunately, no data are available concerning the voluntary activation level in individuals with ID. Nevertheless, the AD in the ID group is similar in magnitude to deficits reported for the quadriceps femoris in some individuals with central nervous system disorders. This AD was at 25–40% in adults after a stroke (Newham & Hsiao, 2001), at 25% in individuals with multiple sclerosis (de Haan, de Ruiter, van der Woude, & Jongen, 2000), and at 33% in individuals with cerebral palsy (Stackhouse et al., 2005). The voluntary activation failure could be explained by the several central nervous system abnormalities. It has been documented that individuals with ID present a failure of growth and maturation in brain areas during the developmental years (Gabrielli et al., 1998). Post-mortem neuropathological studies in ID showed several alterations in the cerebral cortex structure and in the hippocampus and a reduction in the number of neurons (Dierssen & Ramakers, 2006). Individuals with ID present also dendritic abnormalities (Dierssen & Ramakers, 2006; Fodale, Mafrica, Caminiti, & Grasso, 2006), and neurotransmitter system dysfunction with abnormal neuronal connectivity, resulting in deficient information processing (Kaufmann & Moser, 2000). They present also several abnormalities localized in the white matter tracts that are responsible for the motor function (Yu et al., 2008). The maturational differences in neuromuscular function could be also responsible for the lower central activation level in individuals with ID. Therefore, while our individuals with ID sample are adults (24.9 4.9 years), they demonstrated a voluntary activation level comparable with that
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demonstrated by children without ID (65% vs. 68% respectively) as it has been reported by O’Brien, Reeves, Baltzopoulos, Jones, and Maganaris (2009). In fact, ID is defined as a condition of arrest or incomplete development of the mind, which does not only affect cognitive functions, but motor functions as well (World Health Organization, 2007). An inactive lifestyle could be an important factor of this lower central voluntary activation because individuals with ID are less active than general population (Hall & Thomas, 2008). For instance, it has been shown that sedentary individuals without ID have lower voluntary activation than trained ones (Yamada, Kaneko, & Masuda, 2002). Our results showed that individuals with ID present a lower potentiated resting twitch than individuals without ID, which means that they have less muscle volume than individuals without ID. Although muscle size or volume was not directly measured in the present study, the reduced MVC is probably due to muscle atrophy usually reported in individuals with ID (Fryns et al., 1993; Hino-Fukuyo et al., 2006; Van’t Padje et al., 2009), which could be attributed to the inactive lifestyle. Moreover, it seems reasonable to expect that intrinsic muscle properties disorders such as reduced sarcolemmal and/or Ttubules excitability and reduced release of Ca++ from SR may additionally contribute to the lower potentiated twitch reported in individuals with ID. In fact, it has been documented that individuals with ID demonstrate different muscle lactic profile compared to individuals without ID during maximal effort (Chia et al., 2002; Zafeiridis et al., 2010). In the present study, individuals with ID present lower RMS and RMS/Mmax values during MVC than individuals without ID. Nevertheless, no significant difference in the NME ratio was noted between individuals with and without ID. In fact, the NME was defined as ‘‘the responsiveness of muscle to neural excitation’’ (Deschenes et al., 2002). This result suggests that the lower force level is not resulting from functional muscle abnormalities but is related to neural factors. Our results are in line with our previous study (Borji et al., 2013). In this previous study we have reported that, in spite of their lower MVC and lower RMS values, individuals with ID present similar NME values with individuals without ID. Moreover, some studies established a relationship between muscle force level and different incapacities in individuals with ID such as cardiovascular reduced capacities (Pitetti & Boneh, 1995), and lower anaerobic power (Chia et al., 2002; Zafeiridis et al., 2010). In addition, some studies demonstrated that the force deficit in individuals with ID is strongly related to the degree of hypotonia reported in these individuals (Morris, Vaughan, & Vacarro, 1982). There are some limitations that should be addressed. First, while statistical analysis demonstrated no significant difference on BMI between groups, we have not measured the % of body fat for both groups. In this context, it should be noted, that EMG signal may be affected by body fat and skinfold thickness individual differences (Nordander et al., 2003). Second, the original twitch interpolation technique described by Merton (1954) and subsequently employed by many others (Belanger & McComas, 1981; Bigland-Ritchie, Furbush & Woods, 1986) involved a single stimulus interpolated over voluntary contractions. However, recently, it has become common for two or more stimuli (50–100 Hz) to be employed because the evoked force increments are larger and more readily detected (Strojnik, 1995; Suter & Herzog, 2001). Moreover, it has been reported that supramaximal twin, triple and quadruple stimuli (at 125 Hz) evoke less variable force increments than single stimuli (Suter & Herzog, 2001). Finally, although the twitch interpolation technique is an efficient technique to explore voluntary activation, spinal and supraspinal contributions on the AD in individuals with ID are still unknown. Future study should explore cortical activation in individuals with ID during exercise using the transcranial magnetic stimulation. 5. Conclusion The results of our study showed that individuals with ID have lower ability to activate their motor units. Moreover, our study showed a muscle structure difference between individuals with and without ID. These results could have important implications for coaches of ID athletes. They should focus on neuromuscular function improvement in order to increase the nervous system efficiency to activate motor unit. As in individuals without ID, neuromuscular function and muscle structure improvement could be possible in individuals with ID by inserting strength training program in their physical activities. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgements The authors would like to thank all participants for their understanding and availability. Special gratitude is due to all collaborating and volunteers of the Tunisian Union of Aid to Mental Insufficiency (TUAMI) for their contribution in this study. References American Psychiatric Association (2000). Diagnostic and statistical manual of mental disorders (4th ed. (DSM-IV)). Washington, DC: American Psychiatric Association. Angelopoulou, N., Tsimaras, V., Christoulas, K., Kokaridas, D., & Mandroukas, K. (1999). Isokinetic knee muscle strength of individuals with mental retardation, a comparative study. Perceptual and Motor Skills, 88(3 Pt 1), 849–855. Babault, N., Pousson, M., Ballay, Y., & Van Hoecke, J. (2001). Activation of human quadriceps femoris during isometric, concentric, and eccentric contractions. Journal of Applied Physiology, 91, 2628–2634. Belanger, A. Y., & McComas, A. J. 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Contents lists available at ScienceDirect
Research in Developmental Disabilities
Individuals with intellectual disability have lower voluntary muscle activation level Rihab Borji a,*, Firas Zghal b, Nidhal Zarrouk c, Sonia Sahli a, Haithem Rebai a a
Unite´ de Recherche Education, Motricite´, Sports et sante´, Institut Supe´rieur du Sport et de l’Education Physique de Sfax, Universite´ de Sfax, Tunisia b Laboratoire Adaptations Me´taboliques a` l’Exercice en Conditions Physiologiques et Pathologiques (AME2P, EA 3533), Universite´ Blaise Pascal, Clermont-Ferrand, France c Laboratoire des techniques d’imagerie me´dicale (LR 12ES06, LTIM), Faculte´ de Me´dicine de Monastir, Universite´ de Monastir, Tunisia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 6 June 2014 Received in revised form 26 August 2014 Accepted 28 August 2014 Available online 20 September 2014
The aim of this study was to explore the voluntary activation level during maximal voluntary contraction (MVC) in individuals with intellectual disability (ID) versus individuals without ID using the twitch interpolation technique. Ten individuals with mild ID (ID group) and 10 sedentary men without ID (control group) participated in this study. The evaluation of neuromuscular function consisted in three brief MVCs (3 s) of the knee extension superimposed with electrical nerve stimulation (NES) to measure voluntary activation. Muscle activity levels were also measured with surface EMG. The root mean square (RMS) was extracted from the EMG signal. The RMS/Mmax ratio and the neuromuscular efficiency (NME) were calculated. Our results reported that individuals with ID present lower muscle strength (p < 0.001), lower voluntary activation level (p < 0.001), lower RMS values of vastus lateralis (p < 0.05), vastus medialis (p < 0.05), and rectus femoris (p < 0.001) muscles. In addition, our results showed lower RMS/Mmax values in the ID group than in the control group for the VM (0.05 0.01 mV vs. 0.04 0.01 mV; p < 0.05) and the RF (0.06 0.02 mV vs. 0.05 0.02 mV; p < 0.05) muscles. However, no significant difference was reported for the VL muscle (0.05 0.02 mV vs. 0.05 0.02 mV; p = 0.463). Moreover, Individuals with ID present smaller potentiated twitch (p < 0.001). However, no significant difference was reported in the NME ratio. These results suggest that the lower muscle strength known in individuals with ID is related to a central nervous system failure to activate motor units and to some abnormal intrinsic muscle properties. It seems that the inactive lifestyle adopted by individuals with ID is one of the most important factors of their lower voluntary activation levels. Therefore, physical activities should be introduced in life style of individuals with ID to improve their neuromuscular function. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Intellectual disability Electrical stimulation Twitch interpolation technique Voluntary activation level Knee extensor muscles
1. Introduction Individuals with intellectual disabilities (ID) present several abnormalities in their nervous system structure (Gabrielli et al., 1998) localized in the white matter tracts that are responsible for the processing of sensory and motor
* Corresponding author at: Institut Supe´rieur de Sport et de l’Education Physique de Sfax, Route de l’Ae´rodroˆme, Km 3.5, BP 1068, 3000 Sfax, Tunisia. Tel.: +216 22092322. E-mail addresses: [email protected] (R. Borji), zghal.fi[email protected] (F. Zghal), [email protected] (N. Zarrouk), [email protected] (S. Sahli), [email protected] (H. Rebai). http://dx.doi.org/10.1016/j.ridd.2014.08.038 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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information (Yu et al., 2008). Several studies have mentioned that individuals with ID present several abnormalities in motor nervous control and neuromuscular coordination (Chia, Lee, & Teo-Koh, 2002). In addition, individuals with ID present lower muscle strength compared to individuals without ID (Angelopoulou, Tsimaras, Christoulas, Kokaridas, & Mandroukas, 1999; Blomqvist, Olsson, Wallin, Wester, & Rehn, 2013; Borji, Sahli, Zarrouk, Zghal, & Rebai, 2013; Carmeli, Ayalon, Barchad, Sheklow, & Reznick, 2002; Horvat, Croce, Pitetti, & Fernhall, 1999). Moreover, in a previous study, we demonstrated that individuals with ID present lower root mean square (RMS) value in comparison with individuals without ID (Borji et al., 2013). Nevertheless, the reason for this force deficiency has not been identified yet. In individuals without ID, it has been demonstrated that muscle force level depends on several factors such as muscular fiber typology (Fitts & Widrick, 1996), training status (Fitts & Widrick, 1996), sex difference (Miller, MacDougall, Tarnopolsky, & Sale, 1993), and age difference (Lindle et al., 1997). Muscle force level depends also on neural mechanisms such as the voluntary activation level of motor units (Gandevia, 2001, 1992). Voluntary activation describes the level of neural drive of muscle during voluntary contractions (Gandevia, Allen, & McKenzie, 1995). One of the methods to evaluate the activation of motor units by the central nervous system is the superimposed twitch technique (Gandevia, 2001; Millet et al., 2012). The presence of a superimposed twitch produced by motor nerve stimulation during a MVC indicates that the whole motor units are not totally recruited by the central nervous system (Merton, 1954). If voluntary activation is incomplete, failure to drive the muscle should occur at or above the site of stimulation of the motor axons (Merton, 1954). Using this technique, many studies have attempted to investigate the relationship between the reduced voluntary force production and the voluntary activation levels in general population (Belanger & McComas, 1981; Bigland-Ritchie, Donovan, & Roussos, 1981), athletic population (Huber, Suter, & Herzog, 1998), and clinical populations (Hurley, Jones, & Newham, 1994; Rutherford, Jones, & Newham, 1986). Studies investigating this relationship in elderly persons and individuals with cerebral palsy found that the lower muscle force noted in both populations had been related to the activation deficit (AD) from central nervous system (Stackhouse et al., 2001; Stackhouse, Binder-Macleod, & Lee, 2005; Yue, Ranganathan, Siemionow, Liu, & Sahgal, 1999). Nevertheless, to our knowledge no data is available about the voluntary activation in individuals with ID. Thus, the aims of this study were to compare the force production and the level of voluntary activation between individuals with ID and individuals without ID as well as to investigate the implication of the central nervous system deficiency in the force production in individuals with ID. 2. Methods 2.1. Participants The sample population consisted of 20 sedentary men who met the same criteria in terms of socioeconomic status and ethnicity. Ten men with ID (age = 24.9 4.9 years; height = 1.7 0.1 m; weight = 77.9 8.3 kg; BMI = 25.7 2.5 kg/m2) participated in the study as an experimental group. The control group consisted of 10 sedentary and healthy (no cardiovascular, metabolic, immunologic, or neuromuscular disorders) men without ID matched for age, height, and weight: (age = 25.2 2.7 years; height = 1.7 0.1 m; weight = 75.3 9.2 kg; BMI = 23.9 1.7 kg/m2). All participants with ID suffered from a mild ID with an intelligence quotient (IQ) between 50 and 55 and 70 (The American Psychiatric Association, 2000) determined by the WAIS-IV test (Wechsler, 2008) elaborated by the educational center psychologist (IQ = 62 3.5). Participants with ID have been recruited randomly from the Tunisian Union of Aid to Mental Insufficiency (TUAMI). The sample excluded individuals with down syndrome, and with multiple disabilities. The participant’s morphological characteristics showed no statistical differences in terms of age, weight, height and BMI between the two groups. The participants were fully informed of the procedure and the risks involved and gave their written consent. The informed consent for the individuals with ID was provided by their parents or legal guardians. 2.2. Study design Three days after a familiarization session with the experimental procedures, participants engaged in the experimental session. The experimental session was preceded by a warm-up consisting of several submaximal contractions (12–15) of knee extension muscles at a freely chosen intensity. The evaluation of neuromuscular function consisted in three brief (3 s) maximal voluntary contractions (MVCs) of the knee extension superimposed with nerve electrical stimulation (NES) to measure voluntary activation. Muscle activity levels were also measured with surface electromyography (EMG). To exclude the confounding effect of fatigue induced by repeated muscular contractions, the three MVCs were separated by a 2-min recovery period. The comparison of data obtained during the first and the third MVC did not reveal any significant difference, suggesting that the experimental procedures did not induce any fatigue. 2.3. Testing procedures and instrumentation 2.3.1. Force measurement The participants performed three MVCs with strong encouragement by the investigator. During testing, the participants were seated on an isometric dynamometer (Good Strength, Metitur, Finland) equipped with a cuff attached to a strain gauge. This cuff was adjusted 2 cm above the lateral malleolus using a Velcro strap. The participants stabilized themselves by
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grasping handles on the side of the chair during contractions. Safety belts were strapped across the chest, thighs and hips to avoid lateral, vertical or frontal displacements. All measurements were taken from the participant’s dominant leg, with the hip and knee angles set at 908 from full extension (= 08). All participants in our study presented the right leg as the dominant leg (determined by the leg used to kick a ball). 2.3.2. Electromyographic recordings The EMG signals of the vastus lateralis (VL), vastus medialis (VM) and rectus femoris (RF) muscles were recorded using bipolar silver chloride surface electrodes (Blue Sensor N-00-S, Ambu, Denmark) during MVC and stimulations. The recording electrodes were taped lengthwise on the skin over the muscle belly following SENIAM recommendations (Hermens, Feriks, Disselhorst-Klug, & Rau, 2000), with an inter-electrode distance of 20 mm. The position of the electrodes was marked on the skin in case they needed to be repositioned during the experiment. The reference electrode was attached to the patella. Low impedance (Z < 5 kV) at the skin-electrode surface was obtained by shaving, abrading the skin with thin sand paper and cleaning with alcohol. EMG signals were amplified (Octal Bio Amp ML 138, ADInstruments, Australia) with a bandwidth frequency ranging from 10 Hz to 1 kHz (common mode rejection ratio > 96 dB, gain = 1000) and simultaneously digitized together with the force signals using an acquisition card (Powerlab 16SP, ADInstruments, Australia) and Labchart 7.0 software (ADInstruments, Australia). The sampling frequency was 2 kHz. MVC force was determined as the peak force reached during maximal efforts. RMS values of the VL, VM and RF EMG activities were calculated during the MVC trials over a 0.5 s period after the force had reached a plateau and before the superimposed stimulation was evoked. Neuromuscular efficiency (NME) was calculated as the ratio of peak force to the sum RMS of the VL, RF, and VM muscles to provide an overall representation of quadriceps muscle group activity (Deschenes et al., 2002; Woods & Bigland-Ritchie, 1983; Zarrouk et al., 2012). 2.3.3. Peripheral nerve stimulation (NES) The twitch interpolation method, proposed by Merton (1954), involves interpolation of a single supramaximal electrical stimulus to the motor nerve during MVC. Voluntary activation is thus quantified by comparing the amplitude of the superimposed twitch with the force evoked by the same stimulus intensity at rest, and immediately following the corresponding MVC (Kufel, Pineda, & Mador, 2002). The femoral nerve was stimulated percutaneously with a single squarewave stimulus of 1 ms duration with maximal voltage of 400 V delivered by a constant current stimulator (Digitimer DS7A, Hertfordshire, United Kingdom). The cathode (self-adhesive electrode: Ag–AgCl, 10 mm diameter) was positioned in the femoral triangle and pressed firmly into place by an experimenter. The anode, a 10 5 cm self-adhesive stimulation electrode (Medicompex SA, Ecublens, Switzerland) was placed midway between the greater trochanter and the iliac crest. Optimal stimulation intensity was determined from M-wave and force measurements before each testing session. Briefly, the stimulation intensity was increased by 5 mA until there was no further increase in either peak twitch force (i.e., the highest value of the knee extension twitch force was reached) or in concomitant VL, VM and RF peak-to-peak M-wave amplitudes (Mmax). During the subsequent testing procedures, the intensity was set to 150% of the optimal intensity to overcome the potential confounding effect of axonal hyperpolarization (Burke, 2002). MVC superimposed with NES were used to calculate the voluntary activation level as follows: 1 superimposed twitch Voluntary activation ð%Þ ¼ 100 potentiated twitch where ‘‘superimposed twitch’’ is the amplitude of the twitch evoked with NES during MVC and ‘‘potentiated twitch’’ is the amplitude of the twitch evoked by a single stimulation delivered 3 s after the end of the MVC. This provided the opportunity to obtain a potentiated mechanical response and so reduce the variability in voluntary activation values (Kufel et al., 2002). The ID group AV was calculated as follows: 1 voluntary activation of ID group AV ð%Þ ¼ 100 voluntary activation of control group 2.4. Statistical analysis All data are presented as means SD and were analyzed by the Statistica for Windows software (version 6.0, StatSoft, Inc., Tulsa, OK). Data distribution normality was confirmed with the Shapiro–Wilk W-test. Independent sample t-tests were executed in order to analyze group differences in characteristics (age, height, weight and BMI), MVC, voluntary activation, potentiated resting twitch, RMS, RMS/Mmax and NME values. The level of significance for all statistical analyses was set at p < 0.05. 3. Results 3.1. Mechanical responses The independent sample t-test demonstrated a significant (p < 0.001) difference in MVC between ID group and control group. Individuals with ID demonstrated lower maximal force producing capacity (439.6 62.7 N vs. 704.1 125.4 N; Fig. 1).
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900 800 700
MVC (N)
600 500 400 300 200 100 0
Controls
ID
Fig. 1. Mean ( SD) values of maximal voluntary contraction (MVC) for individuals with intellectual disability (ID) and those without ID (controls). *** Significant difference at p < 0.001.
Voluntary Activation Level NES (%)
100 90 80 70 60 50 40 30 20 10 0
Contrrols
ID
Fig. 2. Mean ( SD) values of voluntary activation level for individuals with intellectual disability (ID) and those without ID (controls). *** Significant difference at p < 0.001.
Potentiated Resting Twitch (N)
250 200 150 100 50 0
Contro ols
ID
Fig. 3. Mean ( SD) values of potentiated resting twitch (PRT) for individuals with intellectual disability (ID) and those without ID (controls). *** Significant difference at p < 0.001.
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Table 1 Root mean square (RMS), RMS/Mmax values of the vastus lateralis (VL), vastus medialis (VM), and rectus femoris (FR) muscles and neuromuscular efficiency (NME) ratio for individuals with intellectual disability (ID group) and those without ID (controls).
RMS VL (mV) RMS VM (mV) RMS RF (mV) RMS/Mmax VL (mV) RMS/Mmax VM (mV) RMS/Mmax RF (mV) NME
Control group (n = 10) Mean (SD)
ID group (n = 10) Mean (SD)
Independent t-tests (p-value)
0.42 (0.15) 0.51 (0.22) 0.47 (0.17) 0.05 (0.02) 0.05 (0.01) 0.06 (0.02) 536.8 (158.7)
0.27 (0.15) 0.29 (0.07) 0.29 (0.06) 0.05 (0.02) 0.04 (0.01) 0.05 (0.02) 539.3 (144.7)
2.13 2.79 3.02 0.74 2.59 2.55 0.03
(0.046)* (0.012)* (0.007)*** (0.463) (0.018)* (0.020)* (0.970)
* Significant differences at p < 0.05. *** Significant differences at p < 0.001.
In addition, the independent sample t-test indicated a significant (p < 0.001) differences for both voluntary activation and potentiated resting twitch between the ID group and the control group. Individuals with ID presented lower voluntary activation level (65.8 8.0% vs. 85.6 5.0%; Fig. 2) and potentiated resting twitch (115.8 18.9 N vs. 186.3 24.3 N; Fig. 3). 3.2. EMG responses The independent sample t-test indicated significantly lower RMS values in the ID group than the control group for the VL (0.27 0.15 mV vs. 0.42 0.15 mV; p < 0.05), the VM (0.29 0.07 mV vs. 0.51 0.22 mV; p < 0.05), and the RF (0.29 0.06 mV vs. 0.47 0.17 mV; p < 0.001) muscles. Moreover, the independent sample t-test indicated significantly lower RMS/Mmax values in the ID group than the control group for the VM (0.05 0.01 mV vs. 0.04 0.01 mV; p < 0.05) and the RF (0.06 0.02 mV vs. 0.05 0.02 mV; p < 0.05) muscles. However, no significant difference was reported for the VL muscle (0.05 0.02 mV vs. 0.05 0.02 mV; p = 0.463; Table 1). Concerning the NME ratio, the independent sample t-test indicated no significant difference between the ID group and the control group (539.3 144.7 vs.536.8 158.7; p = 0.97; Table 1). 4. Discussion The aims of this study were to compare the force production and the level of voluntary activation between individuals with ID and individuals without ID as well as to investigate the implication of the central nervous system deficiency in the force production in individuals with ID. Our results showed that individuals with ID develop lower MVC than individuals without ID. This result is consistent with previous studies investigating muscle force level in sedentary individuals with ID (Angelopoulou et al., 1999; Borji et al., 2013; Carmeli et al., 2002; Croce, Pitetti, Horvat, & Miller, 1996; Horvat et al., 1999; Pitetti & Boneh, 1995; Zafeiridis et al., 2010). Besides, smaller differences in force level were reported when comparing elite athletes with ID to physical education students without ID (van de Vliet et al., 2006). Moreover, it has been demonstrated that, in individuals without ID, the muscle force level depends on the training status (Fitts & Widrick, 1996) and the voluntary activation level (Gandevia, 2001, 1992). The main result of our study showed that individuals with ID have lower ability to activate motor units than individuals without ID. They were only able to activate 65% of their motor units versus 85% in the control group. Moreover, our ID group presents an AD of 23.13% compared with the control group. Even in individuals without ID, it is well known that the central nervous system fails to generate maximal evocable force (Gandevia, 2001; Strojnik, 1995). Therefore, concerning our control group, our results were in agreement with those of Shield and Zhou (2004) who found that the quadriceps voluntary activation was between 85% and 95% of total motor units in sedentary individuals without ID. Moreover, Babault, Pousson, Ballay, and Van Hoecke (2001) found that the mean activation levels during MVC are 95.2% in individuals practicing regular physical activities. Unfortunately, no data are available concerning the voluntary activation level in individuals with ID. Nevertheless, the AD in the ID group is similar in magnitude to deficits reported for the quadriceps femoris in some individuals with central nervous system disorders. This AD was at 25–40% in adults after a stroke (Newham & Hsiao, 2001), at 25% in individuals with multiple sclerosis (de Haan, de Ruiter, van der Woude, & Jongen, 2000), and at 33% in individuals with cerebral palsy (Stackhouse et al., 2005). The voluntary activation failure could be explained by the several central nervous system abnormalities. It has been documented that individuals with ID present a failure of growth and maturation in brain areas during the developmental years (Gabrielli et al., 1998). Post-mortem neuropathological studies in ID showed several alterations in the cerebral cortex structure and in the hippocampus and a reduction in the number of neurons (Dierssen & Ramakers, 2006). Individuals with ID present also dendritic abnormalities (Dierssen & Ramakers, 2006; Fodale, Mafrica, Caminiti, & Grasso, 2006), and neurotransmitter system dysfunction with abnormal neuronal connectivity, resulting in deficient information processing (Kaufmann & Moser, 2000). They present also several abnormalities localized in the white matter tracts that are responsible for the motor function (Yu et al., 2008). The maturational differences in neuromuscular function could be also responsible for the lower central activation level in individuals with ID. Therefore, while our individuals with ID sample are adults (24.9 4.9 years), they demonstrated a voluntary activation level comparable with that
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demonstrated by children without ID (65% vs. 68% respectively) as it has been reported by O’Brien, Reeves, Baltzopoulos, Jones, and Maganaris (2009). In fact, ID is defined as a condition of arrest or incomplete development of the mind, which does not only affect cognitive functions, but motor functions as well (World Health Organization, 2007). An inactive lifestyle could be an important factor of this lower central voluntary activation because individuals with ID are less active than general population (Hall & Thomas, 2008). For instance, it has been shown that sedentary individuals without ID have lower voluntary activation than trained ones (Yamada, Kaneko, & Masuda, 2002). Our results showed that individuals with ID present a lower potentiated resting twitch than individuals without ID, which means that they have less muscle volume than individuals without ID. Although muscle size or volume was not directly measured in the present study, the reduced MVC is probably due to muscle atrophy usually reported in individuals with ID (Fryns et al., 1993; Hino-Fukuyo et al., 2006; Van’t Padje et al., 2009), which could be attributed to the inactive lifestyle. Moreover, it seems reasonable to expect that intrinsic muscle properties disorders such as reduced sarcolemmal and/or Ttubules excitability and reduced release of Ca++ from SR may additionally contribute to the lower potentiated twitch reported in individuals with ID. In fact, it has been documented that individuals with ID demonstrate different muscle lactic profile compared to individuals without ID during maximal effort (Chia et al., 2002; Zafeiridis et al., 2010). In the present study, individuals with ID present lower RMS and RMS/Mmax values during MVC than individuals without ID. Nevertheless, no significant difference in the NME ratio was noted between individuals with and without ID. In fact, the NME was defined as ‘‘the responsiveness of muscle to neural excitation’’ (Deschenes et al., 2002). This result suggests that the lower force level is not resulting from functional muscle abnormalities but is related to neural factors. Our results are in line with our previous study (Borji et al., 2013). In this previous study we have reported that, in spite of their lower MVC and lower RMS values, individuals with ID present similar NME values with individuals without ID. Moreover, some studies established a relationship between muscle force level and different incapacities in individuals with ID such as cardiovascular reduced capacities (Pitetti & Boneh, 1995), and lower anaerobic power (Chia et al., 2002; Zafeiridis et al., 2010). In addition, some studies demonstrated that the force deficit in individuals with ID is strongly related to the degree of hypotonia reported in these individuals (Morris, Vaughan, & Vacarro, 1982). There are some limitations that should be addressed. First, while statistical analysis demonstrated no significant difference on BMI between groups, we have not measured the % of body fat for both groups. In this context, it should be noted, that EMG signal may be affected by body fat and skinfold thickness individual differences (Nordander et al., 2003). Second, the original twitch interpolation technique described by Merton (1954) and subsequently employed by many others (Belanger & McComas, 1981; Bigland-Ritchie, Furbush & Woods, 1986) involved a single stimulus interpolated over voluntary contractions. However, recently, it has become common for two or more stimuli (50–100 Hz) to be employed because the evoked force increments are larger and more readily detected (Strojnik, 1995; Suter & Herzog, 2001). Moreover, it has been reported that supramaximal twin, triple and quadruple stimuli (at 125 Hz) evoke less variable force increments than single stimuli (Suter & Herzog, 2001). Finally, although the twitch interpolation technique is an efficient technique to explore voluntary activation, spinal and supraspinal contributions on the AD in individuals with ID are still unknown. Future study should explore cortical activation in individuals with ID during exercise using the transcranial magnetic stimulation. 5. Conclusion The results of our study showed that individuals with ID have lower ability to activate their motor units. Moreover, our study showed a muscle structure difference between individuals with and without ID. These results could have important implications for coaches of ID athletes. They should focus on neuromuscular function improvement in order to increase the nervous system efficiency to activate motor unit. As in individuals without ID, neuromuscular function and muscle structure improvement could be possible in individuals with ID by inserting strength training program in their physical activities. 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