An ultrasonographic analysis of the activation patterns of abdominal muscles in children with spastic type cerebral palsy and in typically developing individuals: a comparative study

An ultrasonographic analysis of the activation patterns of abdominal muscles in children with... Background: Abdominal muscles have stiffer appearance in individuals with spastic type cerebral palsy (STCP) than in their typically developing (TD) peers. This apparent stiffness has been implicated in pelvic instability, mal-rotation, poor gait and locomotion. This study was aimed at investigating whether abdominal muscles activation patterns from rest to activity differ in the two groups. Method: From ultrasound images, abdominal muscles thickness during the resting and active stages was measured in 63 STCP and 82 TD children. The thickness at each stage and the change in thickness from rest to activity were compared between the two groups. Results: Rectus abdominis (RA) muscle was the thickest muscle at rest as well as in active stage in both groups. At rest, all muscles were significantly thicker in the STCP children (p < 0.001). From rest to active stages muscle thickness significantly increased (p < 0.001) in the TD group and significantly decreased (p < 0.001) in the STCP children, except for RA, which became thicker during activity in both groups. In active stages, no significant differences in the thickness in the four abdominal muscles were found between the STCP and the TD children. Conclusion: Apart from the RA muscle, the activation pattern of abdominal muscles in individuals with STCP differs from that of TD individuals. Further studies required for understanding the activation patterns of abdominal muscles prior to any physical fitness programmes aimed at improving the quality of life in individuals with STCP. Trial registration: HREC REF: 490/2011. Human Research Ethics Committee, Faculty of Health Sciences, University of Cape Town, South Africa. November 17, 2011. Keywords: Spastic type cerebral palsy (STCP), Abdominal muscles, Muscle thickness, Utra-sound imaging, Rehabilitation Background with spastic type cerebral palsy (STCP), poor postural The abdominal muscles play an important role in stabi- control is noted to be a primary manifestation of the lising the trunk and providing postural stability [1]. motor dysfunction [2]. The need to target the control of These muscles include the internal and external oblique the trunk in therapy as early as possible in children with muscles (IO and EO respectively), the transverse abdom- neurodevelopmental problems has been emphasised by inis (TA) and the rectus abdominis (RA). In children Burtner and co-workers [3]. These authors reported that skeletal muscles possess remarkable plasticity and can quickly gain or lose contractile material according to * Correspondence: saviour.adjenti@yahoo.com; ksdadjenti@ug.edu.gh Department of Anatomy, School of Biomedical & Allied Health Sciences, changes in loading regimens. Therapists often focus, College of Health Sciences, Korle-Bu Campus, University of Ghana, P.O. Box either directly [4] or indirectly [5], on the abdominal KB 143, Korle-Bu, Accra, Ghana muscles for improving postural control and function. Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 2 of 8 Targeting the trunk is particularly common in those Methods children who display an anterior pelvic tilt [4, 6]. This The design of this study was descriptive and analytical. position places a prolonged stretch on the TrA and RA Ethical approval was obtained from the Human Re- muscles needed to maintain a neutral pelvis and subse- search Ethics Committee of the XXXXXXXXXXXXX quently causes inhibition of the stretch reflex [7] thereby (HREC REF: 490/2011). decreasing reactivity in these muscles. Despite the recog- nised clinical importance of these muscles, it is evident Participants from the literature that little is known about the struc- The STCP group was recruited from individuals attend- ture, function and neuronal activity in persons with ing special schools in XXXXXXXX while the TD group STCP [8]. comprises children attending mainstream schools in the Although STCP is a non-progressive disorder, over time vicinity of the special schools. Informed consent and or secondary complications occur due to weakness and tone assent were obtained from individuals and or guardians imbalance [9]. According to Hungerford and co-workers, from these convenient sampling. A learner was excluded the abnormal forces imposed by the muscles on the skel- if he or she had any surgical operation involving the an- etal system result in biomechanical mal-alignment such as terior abdominal wall in the last six months before the the anterior pelvic tilt mentioned above [10]. Additionally, start of the study. in individuals with STCP abnormal recruitment such as For the STCP group, the Gross Motor Function Classi- the top-down recruitment of the trunk muscles is com- fication Scale [GMFCS] [18] was also used by a neurode- mon [11]. This abnormal recruitment has been associated velopmental therapist to determine the level of function with co-contraction of the extremity muscles [7]. Other of the participants to be included. Only children in levels abnormalities noted include a method of fixation of the I-IV formed part of the inclusion criteria. Children at trunk in some STCP population as well as a negligible level V were excluded because they were unable to per- muscular activity in others [10, 12]. With regards to indi- form the test manoeuvres. Another exclusion criterion viduals with STCP, the muscle groups which appear to for individuals with STCP was an involvement with any contribute to this fixation include the flexors, adductors medical treatment that would have impacted on muscle and the internal rotators of the hip, which gives rise to the function (e.g., Botulinum toxin injection, casting, and typical postural and gait patterns seen – couch gait in surgical intervention such as dorsal rhizotomy and bac- diplegia and equines gait in hemiplegia [11]. lofen pump placement) less than six months before the The force-generating capacity of a skeletal muscle and study. consequently muscle strength is reported to be a com- posite function of different aspects of the muscle archi- Assessment tecture, including thickness [13]. Ultrasound imaging is In all participants, anthropometric parameters (i.e. height a non-invasive method of recording changes in muscle and weight were measured before ultrasonographic thickness during activation, which was first exploited in assessment. muscle activity of the myocardium [14]. Ultrasonography A SIEMENS® ACUSONIC X150 ultrasound imaging has since been used to quantify muscle thickness in indi- machine (Munich, Germany) was used to capture the viduals with STCP [15, 16].Ultrasound imaging method thickness of the four abdominal muscles, rectus abdom- has been reported to be fast, inexpensive and above all inis (RA), internal oblique (IO), external oblique (EO) reliable. The advantages of the use of ultrasonography and transverse abdominis (TrA), in both the resting and over electromyography technique have been docu- active stages. To test the muscles in the resting stage, mented by Ohata et al. [16, 17]. children were asked to lie supine on the plinth with no The present study aimed to contribute to the under- activity. For the active stage, children were asked to lie standing of the functioning of abdominal muscles as a supine on the plinth and then asked to perform the fol- group and/or separate muscles of the anterior abdominal lowing activities: (i) To fully abduct the shoulder joint wall in individuals with STCP. The specific objectives of (ii) to tuck in the chin and lift head and neck slightly the study were to: (i) measure the thickness levels in towards the chest; and (iii) to flex the hip as far as pos- each of the four anterior abdominal muscles during the sible. The performance of these activities was aimed at resting and active stages and (ii) compare the changes in initiating a simultaneous contraction of the abdominal thickness, herein referred to as activation pattern muscles, which was then measured. The average of these between these two stages in the two groups. It is three manoeuvres was recorded as the active stage thick- expected that the muscles of TD individuals would dem- ness. The side of active upper or lower limb motion and onstrate greater activation pattern evidenced by a larger of abdominal muscle thickness measurement was the change in thickness from the resting to active stages affected side in hemiplegic children, the right side in than their age-matched peers with STCP. diplegic, quadriplegic and TD children. The principal Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 3 of 8 investigator handled the transducer head (ultra-sound groups. This test was performed by the principal investi- probe) while one of the research assistants, a neurodeve- gator (SKA) on different occasions. Measurements were lopmental therapist, issued the instructions to the taken at three different points for a particular muscle participants. per participant and the averages were recorded. In each Using the umbilicus as a landmark the ultrasound participant, muscle thickness was measured as described probe was placed two to three centimetres from the above, in both the resting and active stages by SKA. The midline and then was panned around in a semi-circular same assessor repeated the measurements one week fashion until the bulk of the image from the deepest later. The outcome of this intra-rater reliability test was lying abdominal muscle, TrA, was observed on the expressed as reliability indexes (Intraclass Correlation image screen. This position was marked on the skin with Coefficient, typical error and mean differences ± SD be- a marker pen in order to ensure that the probe was kept tween the measures taken by the two assessments), in this position for subsequent measurements. The scan- showing good to excellent correlation (ICC ≥ 0.80) see ning head of the probe was then oriented along the Tables 4 and 5 in Appendix). mid-sagittal axis of each of the rest of the three antero- lateral abdominal muscle (EO, IO and TrA) in a some- Statistical analysis what oblique fashion. The pressure of the transducer STATISTICA software package, version 11 (2012) was was kept to a minimum by using a generous amount of used to analyse the data. The BMI was calculated using the contact gel in order to obtain optimum values for the standard formula, mass (kg)/height (m) x height (m) muscle thickness. All sites along a muscle from which [19]. Descriptive statistics were presented for the data images were taken at rest were then repeated during sets: height, weight, age and muscle thickness. Due to each child’s head and shoulder/leg lift movement (active the relatively large sample size, normality was assumed stage). Images were stored on a personal computer and and parametric tests were used for all analyses. The then analysed with ImageJ Microsoft version 1.46, 2011 Chi-Square test was used to compare the sex distribu- edition (Richmond, Virginia, USA). tion between the STCP and TD groups. Independent Muscle thickness (MT) was determined using an elec- t-test was used to statistically compare the means of the tronic calliper on a frozen image. The length of a per- two groups in both resting and active stages. A two-way pendicular line drawn between the echoes parallel to the ANOVA with repeated measures was used to determine fascicles from the deep up to the superficial aponeurosis if there was a significant group-stage interaction that af- (inter-fascial planes) was measured (Fig. 1). Since thick- fected muscle thickness. The changes in muscle thick- ness varies along the length of a muscle, measurements ness from rest to the active stage in each group were were taken at three different points for a particular compared using paired t-test. A 95% confidence interval muscle according to the clarity of the image and the was used to determine the precision of the estimates of average was recorded for that individual. the differences in muscle thickness between the resting Before the test, the intra-rater reliability of the ultra- and active stages for both groups. Association between sound measurements was assessed on fifteen (15) muscle thickness and age of all participants was assessed randomly selected participants in the STCP and TD using the Pearson’s correlation coefficient. The level of significance for all statistical tests was set at 0.05. Results Over 200 participants (more than 100 in each group) met the inclusion criteria and were invited to participate. The parents of 145 (63 children with STCP and 82 TD children) gave consent and their children were recruited. The demographic data of all the participants are shown in Table 1. There were no significant differences in age (p = 0.102) and in gender (X = 0.139; p = 0.709) between the two groups (STCP group: mean age 11.2 ± 2.9 years, 55.6% males: TD group: mean age 11.3 ± 2.9 years, 52.4% males). The groups were also similar as regards height and weight. `However, the children with STCP were both shorter and heavier than the children in the TD Fig. 1 Sonogram showing the three anterolateral muscles. SF = skin group, and therefore they had a significantly greater and superficial fascia, AC = abdominal cavity. The RA is out of view BMI (p < 0.001). Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 4 of 8 Table 1 Comparison of demographic data between the groups STCP TD t-value Df p-value Mean SD Mean SD Age (years) 11.89 2.92 11.05 2.92 1.65 143 0.102 Height (cm) 139.19 16.04 143.32 17.13 −1.48 143 0.142 Weight (kg) 39.68 10.28 38.75 12.38 0.48 143 0.629 −2 BMI (kg.m ) 20.14 2.16 18.37 2.62 4.34 143 < 0.001 The distribution of the various subtypes of the spastic cerebral palsy is shown in Table 2.Morethanhalf(N = 34) of the STCP participants were able to move independently without appliances (GMFCS level I). There were between eight and eleven children in each of the other levels. Forty-four of the participants had hemiplegia (Table 2). Muscle thickness at rest showed a significant positive Fig. 2 Scatterplot diagrams of age of participants and mean resting muscle thickness for both groups combined (N = 145), showing association with the age of participants (r = 0.766–0.864, Pearson’s correlation (r) between muscles thickness and age. All p < 0.001) in both groups (Fig. 2). The RA muscle correlation coefficients were significant at p < 0.001. EO = external remained the thickest muscle across all ages in both oblique; IO = external oblique; TrA = transversus abdominis; groups, followed by the IO, EO and TrA muscles. RA = rectus abdominis The average thickness of each muscle at rest and the active stages in the two groups and the results of paired and unpaired t-tests are reported in Table 3. Data are and then decreased in thickness when the active ma- also shown graphically in Figs. 3, 4, 5 and 6. At rest, all noeuvres were performed. The RA muscle of the STCP muscles were significantly thicker in the STCP than in group resembled those of TD children in both thickness the TD children (p < 0.001). From rest to active stages, and activation patterns. It may be that the abdominal muscle thickness significantly increased (p < 0.001) in muscles have to stabilise the multi-jointed spine and the TD group and significantly decreased (p < 0.001) in pelvis even in supine position, which requires both con- the STCP children, except for RA, which became thicker centric and eccentric contraction, compared to the com- during activity in both groups. The repeated measures paratively simple task of controlling one or two joints in ANOVA confirmed the signicant (p < 0.001) group x the case of the lower limb muscles. Therefore, since in- stage interaction effect on thickness for all muscles (EO: F dividuals with STCP require more support of the trunk (1,143) = 283.097; IO: 310.669; TrA: 601.925; RA: 25.278). than their TD counterparts, the trunk stabilising role In active stages, no significant difference in the thickness could inevitably predispose the abdominal muscles in of the four abdominal muscles was found between the individuals with STCP to become relatively thicker at STCP and TD children, and the RA muscle was still the rest than for the TD group. Ohata and co-workers also thickest muscle in both groups. found the abdominal muscles thickness in individuals with STCP to be remarkably high at rest [20]. Apart Discussion from the work of Ohata and co-workers [20], no other The counterintuitive results that emerged from the study comparable results for the abdominal muscles in STCP were that apart from the RA, the muscles of the STCP children are found in the literature. were thicker at rest, than the muscles of the TD children The size of the RA, the thickest muscle in both groups, may be explained in terms of postural roles. Although recruitment patterns differ between individuals Table 2 Gross Motor Classification System Level per distribution and are influenced by changes in body position, a thicker of STCP (N = 63) RA than the rest of the abdominal muscles could prob- LEVEL Hemiplegia Diplegia Quadriplegia Total for level ably be a result of the use this muscle in all global move- I29 5 0 34 ments of the trunk during activity of daily living [21]. It II 9 2 0 11 has been suggested that the abdominal muscles may be III 3 4 1 8 in constant state of contraction, either due to neuro- IV 3 3 4 10 logical damage leading to spasticity/hypertonia or to the need to stabilise the trunk in the presence of deficient All Groups 44 14 5 63 postural responses [2]. A related study which focused on Note the high distribution of the hemiplegic subtypes of STCP in this study Note also that only four disability levels (ambulatory individuals) were recruited the neuromuscular activity of the abdominal muscles, Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 5 of 8 Table 3 Comparison of average raw muscle thickness at rest and active stage in both STCP and TD groups Rest Activity Mean diff. T-statistic p-value 95% CI of diff. EO STCP 3.64 ± 0.50 3.36 ± 0.52 0.28 12.43 < 0.001 0.24 to 0.32 TD 3.08 ± 0.50 3.29 ± 0.50 −0.21 −11.21 < 0.001 −0.24 to − 0.18 Mean diff. 0.56 0.08 95% CI of diff. 0.47 to 0.65 0.00 to 0.16 p-value < 0.001 0.086 IO STCP 4.76 ± 0.69 4.43 ± 0.73 0.33 11.04 < 0.001 0.27 to 0.38 TD 4.25 ± 0.52 4.45 ± 0.52 −0.20 −15.35 < 0.001 −0.23 to −0.17 Mean diff. 0.51 −0.02 95% CI of diff. 0.40 to 0.62 −0.12 to 0.08 p-value < 0.001 0.104 TrA STCP 2.86 ± 0.49 2.56 ± 0.48 0.30 16.30 < 0.001 0.27 to 0.33 TD 2.10 ± 0.53 2.38 ± 0.49 −0.28 −18.49 < 0.001 −0.31 to − 0.25 Mean diff. 0.76 0.18 95% CI of diff. 0.66 to 0.86 0.10 to 0.26 p-value < 0.001 0.082 RA STCP 6.33 ± 0.91 6.70 ± 0.93 −0.37 −17.65 < 0.001 −0.41 to −0.33 TD 5.44 ± 0.59 5.97 ± 0.63 −0.53 −23.97 < 0.001 −0.57 to − 0.49 Mean diff. 0.89 0.73 95% CI of diff. 0.75 to 1.03 0.59 to 0.87 p-value < 0.001 0.130 EO external oblique muscle, IO internal oblique muscle, TrA transverse abdominis muscle, RA rectus abdominis muscle, STCP spastic type cerebral palsy, TD typically developing developing, diff. difference reported high EMG activation patterns during periods of in a state of contraction formerly at rest. However, with inactivity (resting stage) in a cohort of children and ado- the exception of RA, muscle thickness in the STCP lescents with STCP [2]. Such evidence would support group was less when active than during the resting stage, the result from the present study and suggests that the indicating that these other abdominal muscles might dif- levels of abdominal muscles thickness at rest may have fer structurally and functionally from those of TD indi- underlying physiological/neurological activity, which viduals. Although similar decrease in abdominal muscle needs further investigation. This physiological/neuro- thickness from resting to active stage was reported by logical activity would also partially explain why the mus- Ohata et al. [20], further investigations would be cles in the STCP group showed less change during neck required to fully understand the anatomy and physiology and lower/upper limb activity, as they might have been of these muscles in individuals with STCP. Fig. 3 Error bar plots showing the mean thickness for the external Fig. 4 Error bar plots showing the mean thickness for the internal oblique muscle (EO) during resting and active stages in both groups. oblique muscle (IO) during resting and active stages in both groups. STCP = spastic type cerebral palsy; TD = typically developing STCP = spastic type cerebral palsy; TD = typically developing Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 6 of 8 ability to activate the contractile materials optimally as a decrease in thickness from resting to active stages was ob- served. Alternatively, a varying amount of non-contractile materials in these muscles might have contributed to the differences in thickness between the two groups. An inclu- sion of this aspect in further investigation would be useful for a better understanding. This study has some limitations. First more than two-third ( / ) of the children with STCP enrolled were hemiplegic and more than half were at the highest func- tional level. These proportions limit the generalisation of ourfinding sincetheyare higher than thosein epidemiological studies [23]. This discrepancy may be due Fig. 5 Error bar plots showing the mean thickness for the transverse to the sampling from special schools in which only educ- abdominis muscle (TrA) during resting and active stages in both groups. STCP = spastic type cerebral palsy; TD = typically developing able children are admitted and more severe disability levels, which are associated with severe mental involvement [24], are excluded. Moreover, the researcher who analysed the In both groups, the level of thickness and activation images was not blinded and this may have introduced some pattern of the RA muscle suggest that this muscle may bias. be suitable to take on the stabilising and flexing role of Finally, in the children with STCP, the chosen neutral the other abdominal muscles on activity. In individuals (plinth) position might not reflect the true thickness of with STCP, the activation pattern of the RA muscle abdominal muscles at rest. Actually, in children with might result from the inhibition of the other abdominal some neuromuscular deficit the abdominal muscles muscles that decreased their level of contraction during might have been conditioned to contract also in that activity. From a functional perspective, weak and inad- position in an attempt to stabilise the spine and pelvis. equately contracting oblique muscles are often associ- ated with a lack of trunk rotation and an accompanying Conclusion altered gait, all features that characterise individuals with The resting stage thickness of the anterior abdominal wall STCP. It could therefore, be inferred from the results of muscles of individuals with STCP is greater than those of this study that the function of trunk rotation by the EO their TD counterparts. The change in muscle thickness of and IO muscles in individuals with STCP could be sacri- abdominal muscles from the resting to active stages in in- ficed above the need to stabilise the trunk. The latter dividuals with STCP differs from that of TD children ex- role taken on almost exclusively by the RA muscle: a cept for the RA muscle, thereby implying that the RA trunk flexor with no rotatory moment on activity [22]. muscle is unaffected or less affected by the condition. This The larger thickness found at rest in children with STCP knowledge could be useful in the problem-solving ap- in comparison with their TD counterparts might potentially proaches with regard to the functional aspect of the mus- indicate muscle hypertrophy. In that case, however, except culoskeletal system in the provision of quality-of-life for the RA muscle, children with STCP seem lack the benefits for individuals with STCP. Further research is needed to examine the patterns of abdominal muscle ac- tivity through dynamic electromyography (EMG). Highlights of this study include In children with STCP, the activation patterns of abdominal muscles, except for the RA differ from those found in TD children. Apart from the RA, the rest of the abdominal muscles in children with STCP are thicker at rest than during the active stage which might indicate hypertonicity or increased need to stabilise the trunk. Fig. 6 Error bar plots showing the mean thickness for the rectus The role of abdominal muscles in stabilising the abdominis muscle (RA) during resting and active stages in both trunk / pelvis in individuals with STCP requires groups. STCP = spastic type cerebral palsy; TD = typically developing further investigation. Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 7 of 8 Appendix Availability of data and materials The datasets used and/or analysed during the current study are available Table 4 Intra-rater reliability of the ultrasound measurements from the corresponding author on reasonable request. (direct method) in the feasibility study for the STCP group (n = 15). Authors’ contributions Data were expressed as typical error and intra-class coefficients The conception of this research idea was by JJ, a Physiotherapist. (ICC) with their 95% confidence intervals (CI) and mean differences Accessibility to participants and equipment was overseen by MU, also a ±standarddeviation (SD) Physiotherapist. Recruitment of the participants and collection of data were carried out by SKA as his doctoral research. The analysis of the data was Muscle & Stage Typical Error 95% CI ICC 95% CI Mean diff ± SD undertaken by JJ and SKA. The drafting and editing of the manuscript was EO R 0.65 (0.06–0.24) 0.81 (0.66–0.96) − 0.19 ± 0.04 supervised by GJL. All four authors shared equal responsibilities in the final preparation of the manuscript. All authors read and approved the final EO Ac 0.59 (0.07–0.18) 0.88 (0.76–0.97) −0.10 ± 0.04 manuscript. IO R 0.60 (0.06–0.20) 0.82 (0.86–0.98) 0.10 ± 0.08 IO Ac 0.62 (0.08–0.24) 0.80 (0.65–0.95) 0.11 ± 0.05 Our study is an original research No special grants or financial awards were received for the execution of this TrA R 0.64 (0.05–0.20) 0.82 (0.68–0.98) 0.17 ± 0.07 study. There are no conflicts of interest pertaining to this study and with regard to any of the authors. Strict institutional ethical protocols (University TrA Ac 0.63 (0.06–0.22) 0.85 (0.70–0.94) 0.08 ± 0.06 of Cape Town, Human Research Ethics Committee) were observed. All RA R 0.60 (0.08–0.25) 0.86 (0.75–0.98) −0.11 ± 0.06 individuals and institutions that provided support for this study were fully acknowledged. Limitations to the generalisability of this study were outlined. RA Ac 0.62 (0.07–0.20) 0.88 (0.76–0.97) −0.19 ± 0.03 This manuscript has not been submitted to any other journal for publication. Key: EO R external oblique resting stage, EO Ac external oblique active stage, IO R internal oblique resting stage, IO Ac internal oblique active stage, TrA R Ethics approval and consent to participate transverse abdominis resting. TrA Ac transverse abdominis active stage, RA R Ethics approval and consent to participate in the study was obtained from rectus abdominis resting stage, RA Ac rectus abdominis active stage the Human Research and Ethics Committee (HREC) of the Faculty of Health Sciences, University of Cape Town, Ref. no.: HREC: 490/2011. Table 5 Intra-rater reliability of the ultrasound measurements Consent for publication (direct method) in the feasibility study for the TD group (n = 15). Consent for publication was obtained from the parents/guardian of the Data were expressed as typical error and intra-class coefficients participants. (ICC) with their 95% confidence intervals (CI) and mean differences Competing interests ±standarddeviation (SD) The authors declare that they have no competing interests. The authors Muscle & Stage Typical Error 95% CI ICC 95% CI Mean diff ± SD alone are responsible for the content and writing of this article. EO R 0.62 (0.06–0.22) 0.80 (0.66–0.96) −0.13 ± 0.08 EO Ac 0.60 (0.08–0.20) 0.82 (0.76–0.97) −0.02 ± 0.09 Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in IO R 0.64 (0.05–0.22) 0.81 (0.86–0.98 −0.16 ± 0.06 published maps and institutional affiliations. IO Ac 0.62 (0.06–0.21) 0.79 (0.65–0.95) −0.09 ± 0.08 Author details TrA R 0.64 (0.04–0.20) 0.84 (0.68–0.98) 0.09 ± 0.09 Department of Anatomy, School of Biomedical & Allied Health Sciences, TrA Ac 0.64 (0.06–0.22) 0.85 (0.72–0.94) 0.09 ± 0.09 College of Health Sciences, Korle-Bu Campus, University of Ghana, P.O. Box KB 143, Korle-Bu, Accra, Ghana. Division of Clinical Anatomy & Biological RA R 0.66 (0.08–0.24) 0.85 (0.75–0.98) −0.10 ± 0.09 Anthropology, Department of Human Biology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa. Division of RA Ac 0.63 (0.06–0.20) 0.86 (0.76–0.96) −0.01 ± 0.03 Physiotherapy, Department of Health & Rehabilitation Sciences, Faculty of Key: EO R external oblique resting stage, EO Ac external oblique active stage, Health Sciences, University of Cape Town, Cape Town, South Africa. Division IO R internal oblique resting stage, IO Ac internal oblique active stage, TrA R of Physiotherapy, Faculty of Medicine & Health Sciences, Stellenbosch transverse abdominis resting. TrA Ac transverse abdominis active stage, RA R University, Stellenbosch, South Africa. rectus abdominis resting stage, RA Ac rectus abdominis active stage Received: 16 February 2016 Accepted: 8 May 2018 Abbreviations BMI: Body mass index; CP: Cerebral palsy; EMG: Electromyograph; EO: External oblique muscle; GMFCS: Gross motor function classification References system; IO: Internal oblique muscle; RA: Rectus abdominis muscle; 1. Hodges PW, Eriksson AE, Shierley D, Gandevia SC. Intra-abdominal pressure sEMG: Surface electromyography; STCP: Spastic type cerebral palsy; increases stiffness of the lumbar spine. J Biomech. 2005;38(9):1873–80. TD: Typically developing; TrA: Transversus abdominis muscle 2. Woollacott M, Shunway-Cook A, Hutchinson S, Ciol M, Price R, Kartin D. Effect of balance training on muscle activity used in recovery of stability in children with cerebral palsy: a pilot study. Dev Med Child Neurol. 2005;47: Acknowledgements 455–61. 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Measurement of muscle thickness as quantitative muscle evaluation for adults with cerebral palsy. Phys Ther. 2009;86:1231–9. 17. Benard MR, Becher JG, Harlaar J, Huijing PA, Jaspers RT. Anatomical information is needed in ultrasound imaging of muscle to avoid potentially substantial errors in measurement of muscle geometry. Muscle Nerve. 2009; 39:652–65. 18. Palisano RJ, Rosenbaum P, Bartlett D, Livingston MH. Content validity of the expanded and revised gross motor function classification system. Dev Med Child Neurol. 2008;50(10):744–50. 19. Brener ND, McManus T, Galuska DA, Lowry R, Wechsler H. Reliability and validity of self-reported height and weight among high school students. J Adolesc Health. 2003;32:281–7. 20. Ohata K, Haruta T, Kato T, Nakamura T. Relation between muscle thickness, spasticity, and muscle limitation in children and adolescents with cerebral palsy. Dev Med Child Neurol. 2008;50:152–6. 21. Vasseljen O, Fladmark AM. 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An ultrasonographic analysis of the activation patterns of abdominal muscles in children with spastic type cerebral palsy and in typically developing individuals: a comparative study

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Medicine & Public Health; Physiotherapy; Rehabilitation; Chiropractic Medicine
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Abstract

Background: Abdominal muscles have stiffer appearance in individuals with spastic type cerebral palsy (STCP) than in their typically developing (TD) peers. This apparent stiffness has been implicated in pelvic instability, mal-rotation, poor gait and locomotion. This study was aimed at investigating whether abdominal muscles activation patterns from rest to activity differ in the two groups. Method: From ultrasound images, abdominal muscles thickness during the resting and active stages was measured in 63 STCP and 82 TD children. The thickness at each stage and the change in thickness from rest to activity were compared between the two groups. Results: Rectus abdominis (RA) muscle was the thickest muscle at rest as well as in active stage in both groups. At rest, all muscles were significantly thicker in the STCP children (p < 0.001). From rest to active stages muscle thickness significantly increased (p < 0.001) in the TD group and significantly decreased (p < 0.001) in the STCP children, except for RA, which became thicker during activity in both groups. In active stages, no significant differences in the thickness in the four abdominal muscles were found between the STCP and the TD children. Conclusion: Apart from the RA muscle, the activation pattern of abdominal muscles in individuals with STCP differs from that of TD individuals. Further studies required for understanding the activation patterns of abdominal muscles prior to any physical fitness programmes aimed at improving the quality of life in individuals with STCP. Trial registration: HREC REF: 490/2011. Human Research Ethics Committee, Faculty of Health Sciences, University of Cape Town, South Africa. November 17, 2011. Keywords: Spastic type cerebral palsy (STCP), Abdominal muscles, Muscle thickness, Utra-sound imaging, Rehabilitation Background with spastic type cerebral palsy (STCP), poor postural The abdominal muscles play an important role in stabi- control is noted to be a primary manifestation of the lising the trunk and providing postural stability [1]. motor dysfunction [2]. The need to target the control of These muscles include the internal and external oblique the trunk in therapy as early as possible in children with muscles (IO and EO respectively), the transverse abdom- neurodevelopmental problems has been emphasised by inis (TA) and the rectus abdominis (RA). In children Burtner and co-workers [3]. These authors reported that skeletal muscles possess remarkable plasticity and can quickly gain or lose contractile material according to * Correspondence: saviour.adjenti@yahoo.com; ksdadjenti@ug.edu.gh Department of Anatomy, School of Biomedical & Allied Health Sciences, changes in loading regimens. Therapists often focus, College of Health Sciences, Korle-Bu Campus, University of Ghana, P.O. Box either directly [4] or indirectly [5], on the abdominal KB 143, Korle-Bu, Accra, Ghana muscles for improving postural control and function. Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 2 of 8 Targeting the trunk is particularly common in those Methods children who display an anterior pelvic tilt [4, 6]. This The design of this study was descriptive and analytical. position places a prolonged stretch on the TrA and RA Ethical approval was obtained from the Human Re- muscles needed to maintain a neutral pelvis and subse- search Ethics Committee of the XXXXXXXXXXXXX quently causes inhibition of the stretch reflex [7] thereby (HREC REF: 490/2011). decreasing reactivity in these muscles. Despite the recog- nised clinical importance of these muscles, it is evident Participants from the literature that little is known about the struc- The STCP group was recruited from individuals attend- ture, function and neuronal activity in persons with ing special schools in XXXXXXXX while the TD group STCP [8]. comprises children attending mainstream schools in the Although STCP is a non-progressive disorder, over time vicinity of the special schools. Informed consent and or secondary complications occur due to weakness and tone assent were obtained from individuals and or guardians imbalance [9]. According to Hungerford and co-workers, from these convenient sampling. A learner was excluded the abnormal forces imposed by the muscles on the skel- if he or she had any surgical operation involving the an- etal system result in biomechanical mal-alignment such as terior abdominal wall in the last six months before the the anterior pelvic tilt mentioned above [10]. Additionally, start of the study. in individuals with STCP abnormal recruitment such as For the STCP group, the Gross Motor Function Classi- the top-down recruitment of the trunk muscles is com- fication Scale [GMFCS] [18] was also used by a neurode- mon [11]. This abnormal recruitment has been associated velopmental therapist to determine the level of function with co-contraction of the extremity muscles [7]. Other of the participants to be included. Only children in levels abnormalities noted include a method of fixation of the I-IV formed part of the inclusion criteria. Children at trunk in some STCP population as well as a negligible level V were excluded because they were unable to per- muscular activity in others [10, 12]. With regards to indi- form the test manoeuvres. Another exclusion criterion viduals with STCP, the muscle groups which appear to for individuals with STCP was an involvement with any contribute to this fixation include the flexors, adductors medical treatment that would have impacted on muscle and the internal rotators of the hip, which gives rise to the function (e.g., Botulinum toxin injection, casting, and typical postural and gait patterns seen – couch gait in surgical intervention such as dorsal rhizotomy and bac- diplegia and equines gait in hemiplegia [11]. lofen pump placement) less than six months before the The force-generating capacity of a skeletal muscle and study. consequently muscle strength is reported to be a com- posite function of different aspects of the muscle archi- Assessment tecture, including thickness [13]. Ultrasound imaging is In all participants, anthropometric parameters (i.e. height a non-invasive method of recording changes in muscle and weight were measured before ultrasonographic thickness during activation, which was first exploited in assessment. muscle activity of the myocardium [14]. Ultrasonography A SIEMENS® ACUSONIC X150 ultrasound imaging has since been used to quantify muscle thickness in indi- machine (Munich, Germany) was used to capture the viduals with STCP [15, 16].Ultrasound imaging method thickness of the four abdominal muscles, rectus abdom- has been reported to be fast, inexpensive and above all inis (RA), internal oblique (IO), external oblique (EO) reliable. The advantages of the use of ultrasonography and transverse abdominis (TrA), in both the resting and over electromyography technique have been docu- active stages. To test the muscles in the resting stage, mented by Ohata et al. [16, 17]. children were asked to lie supine on the plinth with no The present study aimed to contribute to the under- activity. For the active stage, children were asked to lie standing of the functioning of abdominal muscles as a supine on the plinth and then asked to perform the fol- group and/or separate muscles of the anterior abdominal lowing activities: (i) To fully abduct the shoulder joint wall in individuals with STCP. The specific objectives of (ii) to tuck in the chin and lift head and neck slightly the study were to: (i) measure the thickness levels in towards the chest; and (iii) to flex the hip as far as pos- each of the four anterior abdominal muscles during the sible. The performance of these activities was aimed at resting and active stages and (ii) compare the changes in initiating a simultaneous contraction of the abdominal thickness, herein referred to as activation pattern muscles, which was then measured. The average of these between these two stages in the two groups. It is three manoeuvres was recorded as the active stage thick- expected that the muscles of TD individuals would dem- ness. The side of active upper or lower limb motion and onstrate greater activation pattern evidenced by a larger of abdominal muscle thickness measurement was the change in thickness from the resting to active stages affected side in hemiplegic children, the right side in than their age-matched peers with STCP. diplegic, quadriplegic and TD children. The principal Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 3 of 8 investigator handled the transducer head (ultra-sound groups. This test was performed by the principal investi- probe) while one of the research assistants, a neurodeve- gator (SKA) on different occasions. Measurements were lopmental therapist, issued the instructions to the taken at three different points for a particular muscle participants. per participant and the averages were recorded. In each Using the umbilicus as a landmark the ultrasound participant, muscle thickness was measured as described probe was placed two to three centimetres from the above, in both the resting and active stages by SKA. The midline and then was panned around in a semi-circular same assessor repeated the measurements one week fashion until the bulk of the image from the deepest later. The outcome of this intra-rater reliability test was lying abdominal muscle, TrA, was observed on the expressed as reliability indexes (Intraclass Correlation image screen. This position was marked on the skin with Coefficient, typical error and mean differences ± SD be- a marker pen in order to ensure that the probe was kept tween the measures taken by the two assessments), in this position for subsequent measurements. The scan- showing good to excellent correlation (ICC ≥ 0.80) see ning head of the probe was then oriented along the Tables 4 and 5 in Appendix). mid-sagittal axis of each of the rest of the three antero- lateral abdominal muscle (EO, IO and TrA) in a some- Statistical analysis what oblique fashion. The pressure of the transducer STATISTICA software package, version 11 (2012) was was kept to a minimum by using a generous amount of used to analyse the data. The BMI was calculated using the contact gel in order to obtain optimum values for the standard formula, mass (kg)/height (m) x height (m) muscle thickness. All sites along a muscle from which [19]. Descriptive statistics were presented for the data images were taken at rest were then repeated during sets: height, weight, age and muscle thickness. Due to each child’s head and shoulder/leg lift movement (active the relatively large sample size, normality was assumed stage). Images were stored on a personal computer and and parametric tests were used for all analyses. The then analysed with ImageJ Microsoft version 1.46, 2011 Chi-Square test was used to compare the sex distribu- edition (Richmond, Virginia, USA). tion between the STCP and TD groups. Independent Muscle thickness (MT) was determined using an elec- t-test was used to statistically compare the means of the tronic calliper on a frozen image. The length of a per- two groups in both resting and active stages. A two-way pendicular line drawn between the echoes parallel to the ANOVA with repeated measures was used to determine fascicles from the deep up to the superficial aponeurosis if there was a significant group-stage interaction that af- (inter-fascial planes) was measured (Fig. 1). Since thick- fected muscle thickness. The changes in muscle thick- ness varies along the length of a muscle, measurements ness from rest to the active stage in each group were were taken at three different points for a particular compared using paired t-test. A 95% confidence interval muscle according to the clarity of the image and the was used to determine the precision of the estimates of average was recorded for that individual. the differences in muscle thickness between the resting Before the test, the intra-rater reliability of the ultra- and active stages for both groups. Association between sound measurements was assessed on fifteen (15) muscle thickness and age of all participants was assessed randomly selected participants in the STCP and TD using the Pearson’s correlation coefficient. The level of significance for all statistical tests was set at 0.05. Results Over 200 participants (more than 100 in each group) met the inclusion criteria and were invited to participate. The parents of 145 (63 children with STCP and 82 TD children) gave consent and their children were recruited. The demographic data of all the participants are shown in Table 1. There were no significant differences in age (p = 0.102) and in gender (X = 0.139; p = 0.709) between the two groups (STCP group: mean age 11.2 ± 2.9 years, 55.6% males: TD group: mean age 11.3 ± 2.9 years, 52.4% males). The groups were also similar as regards height and weight. `However, the children with STCP were both shorter and heavier than the children in the TD Fig. 1 Sonogram showing the three anterolateral muscles. SF = skin group, and therefore they had a significantly greater and superficial fascia, AC = abdominal cavity. The RA is out of view BMI (p < 0.001). Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 4 of 8 Table 1 Comparison of demographic data between the groups STCP TD t-value Df p-value Mean SD Mean SD Age (years) 11.89 2.92 11.05 2.92 1.65 143 0.102 Height (cm) 139.19 16.04 143.32 17.13 −1.48 143 0.142 Weight (kg) 39.68 10.28 38.75 12.38 0.48 143 0.629 −2 BMI (kg.m ) 20.14 2.16 18.37 2.62 4.34 143 < 0.001 The distribution of the various subtypes of the spastic cerebral palsy is shown in Table 2.Morethanhalf(N = 34) of the STCP participants were able to move independently without appliances (GMFCS level I). There were between eight and eleven children in each of the other levels. Forty-four of the participants had hemiplegia (Table 2). Muscle thickness at rest showed a significant positive Fig. 2 Scatterplot diagrams of age of participants and mean resting muscle thickness for both groups combined (N = 145), showing association with the age of participants (r = 0.766–0.864, Pearson’s correlation (r) between muscles thickness and age. All p < 0.001) in both groups (Fig. 2). The RA muscle correlation coefficients were significant at p < 0.001. EO = external remained the thickest muscle across all ages in both oblique; IO = external oblique; TrA = transversus abdominis; groups, followed by the IO, EO and TrA muscles. RA = rectus abdominis The average thickness of each muscle at rest and the active stages in the two groups and the results of paired and unpaired t-tests are reported in Table 3. Data are and then decreased in thickness when the active ma- also shown graphically in Figs. 3, 4, 5 and 6. At rest, all noeuvres were performed. The RA muscle of the STCP muscles were significantly thicker in the STCP than in group resembled those of TD children in both thickness the TD children (p < 0.001). From rest to active stages, and activation patterns. It may be that the abdominal muscle thickness significantly increased (p < 0.001) in muscles have to stabilise the multi-jointed spine and the TD group and significantly decreased (p < 0.001) in pelvis even in supine position, which requires both con- the STCP children, except for RA, which became thicker centric and eccentric contraction, compared to the com- during activity in both groups. The repeated measures paratively simple task of controlling one or two joints in ANOVA confirmed the signicant (p < 0.001) group x the case of the lower limb muscles. Therefore, since in- stage interaction effect on thickness for all muscles (EO: F dividuals with STCP require more support of the trunk (1,143) = 283.097; IO: 310.669; TrA: 601.925; RA: 25.278). than their TD counterparts, the trunk stabilising role In active stages, no significant difference in the thickness could inevitably predispose the abdominal muscles in of the four abdominal muscles was found between the individuals with STCP to become relatively thicker at STCP and TD children, and the RA muscle was still the rest than for the TD group. Ohata and co-workers also thickest muscle in both groups. found the abdominal muscles thickness in individuals with STCP to be remarkably high at rest [20]. Apart Discussion from the work of Ohata and co-workers [20], no other The counterintuitive results that emerged from the study comparable results for the abdominal muscles in STCP were that apart from the RA, the muscles of the STCP children are found in the literature. were thicker at rest, than the muscles of the TD children The size of the RA, the thickest muscle in both groups, may be explained in terms of postural roles. Although recruitment patterns differ between individuals Table 2 Gross Motor Classification System Level per distribution and are influenced by changes in body position, a thicker of STCP (N = 63) RA than the rest of the abdominal muscles could prob- LEVEL Hemiplegia Diplegia Quadriplegia Total for level ably be a result of the use this muscle in all global move- I29 5 0 34 ments of the trunk during activity of daily living [21]. It II 9 2 0 11 has been suggested that the abdominal muscles may be III 3 4 1 8 in constant state of contraction, either due to neuro- IV 3 3 4 10 logical damage leading to spasticity/hypertonia or to the need to stabilise the trunk in the presence of deficient All Groups 44 14 5 63 postural responses [2]. A related study which focused on Note the high distribution of the hemiplegic subtypes of STCP in this study Note also that only four disability levels (ambulatory individuals) were recruited the neuromuscular activity of the abdominal muscles, Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 5 of 8 Table 3 Comparison of average raw muscle thickness at rest and active stage in both STCP and TD groups Rest Activity Mean diff. T-statistic p-value 95% CI of diff. EO STCP 3.64 ± 0.50 3.36 ± 0.52 0.28 12.43 < 0.001 0.24 to 0.32 TD 3.08 ± 0.50 3.29 ± 0.50 −0.21 −11.21 < 0.001 −0.24 to − 0.18 Mean diff. 0.56 0.08 95% CI of diff. 0.47 to 0.65 0.00 to 0.16 p-value < 0.001 0.086 IO STCP 4.76 ± 0.69 4.43 ± 0.73 0.33 11.04 < 0.001 0.27 to 0.38 TD 4.25 ± 0.52 4.45 ± 0.52 −0.20 −15.35 < 0.001 −0.23 to −0.17 Mean diff. 0.51 −0.02 95% CI of diff. 0.40 to 0.62 −0.12 to 0.08 p-value < 0.001 0.104 TrA STCP 2.86 ± 0.49 2.56 ± 0.48 0.30 16.30 < 0.001 0.27 to 0.33 TD 2.10 ± 0.53 2.38 ± 0.49 −0.28 −18.49 < 0.001 −0.31 to − 0.25 Mean diff. 0.76 0.18 95% CI of diff. 0.66 to 0.86 0.10 to 0.26 p-value < 0.001 0.082 RA STCP 6.33 ± 0.91 6.70 ± 0.93 −0.37 −17.65 < 0.001 −0.41 to −0.33 TD 5.44 ± 0.59 5.97 ± 0.63 −0.53 −23.97 < 0.001 −0.57 to − 0.49 Mean diff. 0.89 0.73 95% CI of diff. 0.75 to 1.03 0.59 to 0.87 p-value < 0.001 0.130 EO external oblique muscle, IO internal oblique muscle, TrA transverse abdominis muscle, RA rectus abdominis muscle, STCP spastic type cerebral palsy, TD typically developing developing, diff. difference reported high EMG activation patterns during periods of in a state of contraction formerly at rest. However, with inactivity (resting stage) in a cohort of children and ado- the exception of RA, muscle thickness in the STCP lescents with STCP [2]. Such evidence would support group was less when active than during the resting stage, the result from the present study and suggests that the indicating that these other abdominal muscles might dif- levels of abdominal muscles thickness at rest may have fer structurally and functionally from those of TD indi- underlying physiological/neurological activity, which viduals. Although similar decrease in abdominal muscle needs further investigation. This physiological/neuro- thickness from resting to active stage was reported by logical activity would also partially explain why the mus- Ohata et al. [20], further investigations would be cles in the STCP group showed less change during neck required to fully understand the anatomy and physiology and lower/upper limb activity, as they might have been of these muscles in individuals with STCP. Fig. 3 Error bar plots showing the mean thickness for the external Fig. 4 Error bar plots showing the mean thickness for the internal oblique muscle (EO) during resting and active stages in both groups. oblique muscle (IO) during resting and active stages in both groups. STCP = spastic type cerebral palsy; TD = typically developing STCP = spastic type cerebral palsy; TD = typically developing Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 6 of 8 ability to activate the contractile materials optimally as a decrease in thickness from resting to active stages was ob- served. Alternatively, a varying amount of non-contractile materials in these muscles might have contributed to the differences in thickness between the two groups. An inclu- sion of this aspect in further investigation would be useful for a better understanding. This study has some limitations. First more than two-third ( / ) of the children with STCP enrolled were hemiplegic and more than half were at the highest func- tional level. These proportions limit the generalisation of ourfinding sincetheyare higher than thosein epidemiological studies [23]. This discrepancy may be due Fig. 5 Error bar plots showing the mean thickness for the transverse to the sampling from special schools in which only educ- abdominis muscle (TrA) during resting and active stages in both groups. STCP = spastic type cerebral palsy; TD = typically developing able children are admitted and more severe disability levels, which are associated with severe mental involvement [24], are excluded. Moreover, the researcher who analysed the In both groups, the level of thickness and activation images was not blinded and this may have introduced some pattern of the RA muscle suggest that this muscle may bias. be suitable to take on the stabilising and flexing role of Finally, in the children with STCP, the chosen neutral the other abdominal muscles on activity. In individuals (plinth) position might not reflect the true thickness of with STCP, the activation pattern of the RA muscle abdominal muscles at rest. Actually, in children with might result from the inhibition of the other abdominal some neuromuscular deficit the abdominal muscles muscles that decreased their level of contraction during might have been conditioned to contract also in that activity. From a functional perspective, weak and inad- position in an attempt to stabilise the spine and pelvis. equately contracting oblique muscles are often associ- ated with a lack of trunk rotation and an accompanying Conclusion altered gait, all features that characterise individuals with The resting stage thickness of the anterior abdominal wall STCP. It could therefore, be inferred from the results of muscles of individuals with STCP is greater than those of this study that the function of trunk rotation by the EO their TD counterparts. The change in muscle thickness of and IO muscles in individuals with STCP could be sacri- abdominal muscles from the resting to active stages in in- ficed above the need to stabilise the trunk. The latter dividuals with STCP differs from that of TD children ex- role taken on almost exclusively by the RA muscle: a cept for the RA muscle, thereby implying that the RA trunk flexor with no rotatory moment on activity [22]. muscle is unaffected or less affected by the condition. This The larger thickness found at rest in children with STCP knowledge could be useful in the problem-solving ap- in comparison with their TD counterparts might potentially proaches with regard to the functional aspect of the mus- indicate muscle hypertrophy. In that case, however, except culoskeletal system in the provision of quality-of-life for the RA muscle, children with STCP seem lack the benefits for individuals with STCP. Further research is needed to examine the patterns of abdominal muscle ac- tivity through dynamic electromyography (EMG). Highlights of this study include In children with STCP, the activation patterns of abdominal muscles, except for the RA differ from those found in TD children. Apart from the RA, the rest of the abdominal muscles in children with STCP are thicker at rest than during the active stage which might indicate hypertonicity or increased need to stabilise the trunk. Fig. 6 Error bar plots showing the mean thickness for the rectus The role of abdominal muscles in stabilising the abdominis muscle (RA) during resting and active stages in both trunk / pelvis in individuals with STCP requires groups. STCP = spastic type cerebral palsy; TD = typically developing further investigation. Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 7 of 8 Appendix Availability of data and materials The datasets used and/or analysed during the current study are available Table 4 Intra-rater reliability of the ultrasound measurements from the corresponding author on reasonable request. (direct method) in the feasibility study for the STCP group (n = 15). Authors’ contributions Data were expressed as typical error and intra-class coefficients The conception of this research idea was by JJ, a Physiotherapist. (ICC) with their 95% confidence intervals (CI) and mean differences Accessibility to participants and equipment was overseen by MU, also a ±standarddeviation (SD) Physiotherapist. Recruitment of the participants and collection of data were carried out by SKA as his doctoral research. The analysis of the data was Muscle & Stage Typical Error 95% CI ICC 95% CI Mean diff ± SD undertaken by JJ and SKA. The drafting and editing of the manuscript was EO R 0.65 (0.06–0.24) 0.81 (0.66–0.96) − 0.19 ± 0.04 supervised by GJL. All four authors shared equal responsibilities in the final preparation of the manuscript. All authors read and approved the final EO Ac 0.59 (0.07–0.18) 0.88 (0.76–0.97) −0.10 ± 0.04 manuscript. IO R 0.60 (0.06–0.20) 0.82 (0.86–0.98) 0.10 ± 0.08 IO Ac 0.62 (0.08–0.24) 0.80 (0.65–0.95) 0.11 ± 0.05 Our study is an original research No special grants or financial awards were received for the execution of this TrA R 0.64 (0.05–0.20) 0.82 (0.68–0.98) 0.17 ± 0.07 study. There are no conflicts of interest pertaining to this study and with regard to any of the authors. Strict institutional ethical protocols (University TrA Ac 0.63 (0.06–0.22) 0.85 (0.70–0.94) 0.08 ± 0.06 of Cape Town, Human Research Ethics Committee) were observed. All RA R 0.60 (0.08–0.25) 0.86 (0.75–0.98) −0.11 ± 0.06 individuals and institutions that provided support for this study were fully acknowledged. Limitations to the generalisability of this study were outlined. RA Ac 0.62 (0.07–0.20) 0.88 (0.76–0.97) −0.19 ± 0.03 This manuscript has not been submitted to any other journal for publication. Key: EO R external oblique resting stage, EO Ac external oblique active stage, IO R internal oblique resting stage, IO Ac internal oblique active stage, TrA R Ethics approval and consent to participate transverse abdominis resting. TrA Ac transverse abdominis active stage, RA R Ethics approval and consent to participate in the study was obtained from rectus abdominis resting stage, RA Ac rectus abdominis active stage the Human Research and Ethics Committee (HREC) of the Faculty of Health Sciences, University of Cape Town, Ref. no.: HREC: 490/2011. Table 5 Intra-rater reliability of the ultrasound measurements Consent for publication (direct method) in the feasibility study for the TD group (n = 15). Consent for publication was obtained from the parents/guardian of the Data were expressed as typical error and intra-class coefficients participants. (ICC) with their 95% confidence intervals (CI) and mean differences Competing interests ±standarddeviation (SD) The authors declare that they have no competing interests. The authors Muscle & Stage Typical Error 95% CI ICC 95% CI Mean diff ± SD alone are responsible for the content and writing of this article. EO R 0.62 (0.06–0.22) 0.80 (0.66–0.96) −0.13 ± 0.08 EO Ac 0.60 (0.08–0.20) 0.82 (0.76–0.97) −0.02 ± 0.09 Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in IO R 0.64 (0.05–0.22) 0.81 (0.86–0.98 −0.16 ± 0.06 published maps and institutional affiliations. IO Ac 0.62 (0.06–0.21) 0.79 (0.65–0.95) −0.09 ± 0.08 Author details TrA R 0.64 (0.04–0.20) 0.84 (0.68–0.98) 0.09 ± 0.09 Department of Anatomy, School of Biomedical & Allied Health Sciences, TrA Ac 0.64 (0.06–0.22) 0.85 (0.72–0.94) 0.09 ± 0.09 College of Health Sciences, Korle-Bu Campus, University of Ghana, P.O. Box KB 143, Korle-Bu, Accra, Ghana. Division of Clinical Anatomy & Biological RA R 0.66 (0.08–0.24) 0.85 (0.75–0.98) −0.10 ± 0.09 Anthropology, Department of Human Biology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa. Division of RA Ac 0.63 (0.06–0.20) 0.86 (0.76–0.96) −0.01 ± 0.03 Physiotherapy, Department of Health & Rehabilitation Sciences, Faculty of Key: EO R external oblique resting stage, EO Ac external oblique active stage, Health Sciences, University of Cape Town, Cape Town, South Africa. Division IO R internal oblique resting stage, IO Ac internal oblique active stage, TrA R of Physiotherapy, Faculty of Medicine & Health Sciences, Stellenbosch transverse abdominis resting. TrA Ac transverse abdominis active stage, RA R University, Stellenbosch, South Africa. rectus abdominis resting stage, RA Ac rectus abdominis active stage Received: 16 February 2016 Accepted: 8 May 2018 Abbreviations BMI: Body mass index; CP: Cerebral palsy; EMG: Electromyograph; EO: External oblique muscle; GMFCS: Gross motor function classification References system; IO: Internal oblique muscle; RA: Rectus abdominis muscle; 1. Hodges PW, Eriksson AE, Shierley D, Gandevia SC. Intra-abdominal pressure sEMG: Surface electromyography; STCP: Spastic type cerebral palsy; increases stiffness of the lumbar spine. J Biomech. 2005;38(9):1873–80. TD: Typically developing; TrA: Transversus abdominis muscle 2. Woollacott M, Shunway-Cook A, Hutchinson S, Ciol M, Price R, Kartin D. Effect of balance training on muscle activity used in recovery of stability in children with cerebral palsy: a pilot study. Dev Med Child Neurol. 2005;47: Acknowledgements 455–61. Special thanks to the staff and learners of all the schools from which participants 3. Burtner PA, Qualls C, Woollacott MH. Muscle activation characteristics of were recruited for this study. The authors are also grateful to the technical staff of stance balance control in children with spastic cerebral palsy. Gait Posture. the Division of Clinical Anatomy of the Department of Human Biology, Faculty of 1998;8:163–74. Health Sciences, University of Cape Town, for the transporting of the equipment 4. Unger M, Faure M, Frieg A. Strength training in adolescent learners with to and from the data sampling sites. Finally we appreciate the financial inputs of cerebral palsy: a randomized controlled trial. Clin Rehabil. 2006;20:469–77. both faculty and management of the postgraduate units of the Faculty of Health 5. Prosser LA, Lee SCK, Barbe MF, VanSant AF, Lauer RT. Trunk and hip muscle Sciences of the Universities of Cape Town and Ghana Medical School toward the activity in early walkers with or without cerebral palsy – a frequency doctoral training of the principal investigator. analysis. J Electromyo Kinesiol. 2010;20:851–9. Adjenti et al. Archives of Physiotherapy (2018) 8:9 Page 8 of 8 6. Roussouly P, Gollogly S, Berthonnaud E, Dimnet J. Classification of the normal variation in the sagittal alignment of human lumbar spine and pelvis in the standing position. Spine. 2005;30:346–53. 7. Urquhart DM, Hodges PW, Allen TJ, Story IH. Abdominal muscle recruitment during a range of voluntary exercises. Man Ther. 2005;10(2):144–53. 8. Rose J, McGill KC. Neuromuscular activation and motor-unit firing characteristics in cerebral palsy. Dev Med Child Neurol. 2005;47:329–36. 9. Ando N, Ueda S. Functional deterioration in adults with cerebral palsy. Clin Rehabil. 2000;14:300–6. 10. Hungerford B, Gilleard W, Hodges P. Evidence of altered lumbopelvic muscle recruitment in the presence of sacroiliac joint pain. Spine. 2003;28: 1593–600. 11. Stackhouse SK, Binder-Macleod SA, Lee SCK. Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve. 2005;31:594–601. 12. Ferreira PH, Ferreira ML, Hodges PW. Changes in recruitment of abdominal muscles in people with low back pain: ultrasound measurement of muscle activity. Spine. 2004;29:2560–6. 13. Shortland AP, Harris CA, Gough M, Robinson RO. Architecture of the medial gastrocnemius in children with spastic diplegia. Dev Med Child Neurol. 2002;44:158–63. 14. Heimdal A, Stoylen A, Torp H, Skaerpe T. Real-time strain rate imaging of the left ventricle by ultrasound. J Am Soc Echocardiogr. 1998;11:1013–9. 15. Hodges PW, Pengel LHM, Herbert RD, Gandevia SC. Measurement of muscle contraction with ultrasound imaging. Muscle Nerve. 2003;27:682–92. 16. Ohata K, TsuboyamaT, Ichihashi N, Minami S. Measurement of muscle thickness as quantitative muscle evaluation for adults with cerebral palsy. Phys Ther. 2009;86:1231–9. 17. Benard MR, Becher JG, Harlaar J, Huijing PA, Jaspers RT. Anatomical information is needed in ultrasound imaging of muscle to avoid potentially substantial errors in measurement of muscle geometry. Muscle Nerve. 2009; 39:652–65. 18. Palisano RJ, Rosenbaum P, Bartlett D, Livingston MH. Content validity of the expanded and revised gross motor function classification system. Dev Med Child Neurol. 2008;50(10):744–50. 19. Brener ND, McManus T, Galuska DA, Lowry R, Wechsler H. Reliability and validity of self-reported height and weight among high school students. J Adolesc Health. 2003;32:281–7. 20. Ohata K, Haruta T, Kato T, Nakamura T. Relation between muscle thickness, spasticity, and muscle limitation in children and adolescents with cerebral palsy. Dev Med Child Neurol. 2008;50:152–6. 21. Vasseljen O, Fladmark AM. Abdominal muscle contraction thickness and function after specific and general exercises: a randomised controlled trial in chronic low back pain patients. Man Ther. 2010;15(5):482–9. 22. Andersson EA, Grundstrom H, Thorstensson A. Diverging intramuscular activity patterns in back and abdominal muscles during trunk rotation. Spine. 2002;27(6):e152–60. 23. Gorter JW, Rosenbaum PL, Hanna SE, Palisano RJ, Barlett DJ, Russell DJ, Walter SD, Raina P, Galuppi BE, Wood E. Limb distribution, motor impairment and functional classification of cerebral palsy. Dev Med Child Neurol. 2004;46:461–7. 24. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, Dan B, Jacobson B. A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol. 2007;109(suppl):8–14.

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Archives of PhysiotherapySpringer Journals

Published: Jun 5, 2018

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