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Electrophysiological and histological changes of paraspinal muscles in adolescent idiopathic scoliosis

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  • Charles University in Prague, Third School of Medicine
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Purpose The pathogenesis of adolescent idiopathic scoliosis (AIS) remains poorly understood. To date, potentially involved local changes in the deep paraspinal muscles still remain unknown. Methods Needle electromyography (EMG) and muscle biopsy of paraspinal muscles at convexity and concavity of the AIS main thoracic curve were performed in 25 subjects. In this group, EMG was performed in 16 AIS subjects (12 females, 12–27 years), muscle biopsy in 18 AIS subjects (15 females, 11–31 years) compared to 10 non-scoliotic controls (6 females, 12–55 years). Samples of muscle tissue were removed during corrective surgery and were examined histologically, enzyme histochemically and immunohistochemically. Both methods of EMG and muscle biopsy were performed in 9 subjects (7 women, 12–27 years). Results Right curve convexity was found in 24 AIS subjects. Amplitudes of motor unit action potentials (MUPs) were significantly increased on the AIS curve convexity versus concavity. Turns, duration and phases of MUPs were without any significant changes. In all 18 subjects, the histological examination revealed muscle fiber redistribution with numerical predominance of type I on the curve convexity which strongly correlated with the progression of the Cobb angle. Conclusion Our findings demonstrate significant changes of muscle fiber redistribution in the paraspinal muscles of AIS with increased proportion of type I on the convexity corresponding to a significantly higher amplitude of MUPs on the same side. A possible explanation of this alteration is a secondary adaptation due to chronic high load demand.
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ORIGINAL ARTICLE
Electrophysiological and histological changes of paraspinal
muscles in adolescent idiopathic scoliosis
I. Stetkarova
1
J. Zamecnik
2
V. Bocek
1
P. Vasko
1
K. Brabec
1
M. Krbec
3
Received: 2 December 2015 / Revised: 23 May 2016 / Accepted: 24 May 2016 / Published online: 31 May 2016
ÓSpringer-Verlag Berlin Heidelberg 2016
Abstract
Purpose The pathogenesis of adolescent idiopathic scol-
iosis (AIS) remains poorly understood. To date, potentially
involved local changes in the deep paraspinal muscles still
remain unknown.
Methods Needle electromyography (EMG) and muscle
biopsy of paraspinal muscles at convexity and concavity of
the AIS main thoracic curve were performed in 25 subjects.
In this group, EMG was performed in 16 AIS subjects (12
females, 12–27 years), muscle biopsy in 18 AIS subjects
(15 females, 11–31 years) compared to 10 non-scoliotic
controls (6 females, 12–55 years). Samples of muscle tis-
sue were removed during corrective surgery and were
examined histologically, enzyme histochemically and
immunohistochemically. Both methods of EMG and mus-
cle biopsy were performed in 9 subjects (7 women,
12–27 years).
Results Right curve convexity was found in 24 AIS sub-
jects. Amplitudes of motor unit action potentials (MUPs)
were significantly increased on the AIS curve convexity
versus concavity. Turns, duration and phases of MUPs
were without any significant changes. In all 18 subjects, the
histological examination revealed muscle fiber
redistribution with numerical predominance of type I on
the curve convexity which strongly correlated with the
progression of the Cobb angle.
Conclusion Our findings demonstrate significant changes
of muscle fiber redistribution in the paraspinal muscles of
AIS with increased proportion of type I on the convexity
corresponding to a significantly higher amplitude of MUPs
on the same side. A possible explanation of this alteration
is a secondary adaptation due to chronic high load demand.
Keywords Idiopathic scoliosis Muscle biopsy
Neurophysiology EMG Paraspinal muscles
Introduction
Adolescent idiopathic scoliosis (AIS) is a disease of
unknown etiopathogenesis. There are many theories based
on different principles and there is no doubt that the eti-
ology is multifactorial [1,2]. Neuroadaptive theory
describes the disparity between the growth rate of the
neural tube and axial skeleton of the spine during growth
development [3]. Some authors believe that the main role is
played by disturbances of oculovestibular proprioception
and sensorimotor disintegration in the central nervous
system [4,5]. Connective tissue abnormality, abnormal
biomechanical forces, neurophysiologic predisposition, or
an increase in calmodulin or decrease in melatonin [6]
during puberty are also discussed in the pathophysiology of
this disorder. Apart from epigenetic modification, envi-
ronmental factors may influence idiopathic scoliosis, too
[1].
In AIS, some authors have concentrated on muscle and
peripheral nerve disturbances, but in other studies impair-
ment of the spinal cord and different pattern of brain
&I. Stetkarova
ivana.stetkarova@fnkv.cz
1
Department of Neurology, Third Faculty of Medicine,
Charles University in Prague and Faculty Hospital Kralovske
Vinohrady, Ruska 87, 100 00 Prague 10, Czech Republic
2
Department of Pathology and Molecular Medicine, 2nd
Faculty of Medicine, Charles University in Prague and Motol
University Hospital, Prague, Czech Republic
3
Department of Orthopedics and Traumatology, 3rd Faculty of
Medicine, Charles University in Prague and Faculty Hospital
Kra
´lovske
´Vinohrady, Prague, Czech Republic
123
Eur Spine J (2016) 25:3146–3153
DOI 10.1007/s00586-016-4628-8
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... They found a significant difference in the muscle activation patterns between the two types of physiotherapy exercises. Stetkarova et al. [24] used needle EMG instead of surface EMG (sEMG) to investigate the changes in the paraspinal muscles of AIS patients, and found higher amplitudes of the motor unit potentials on the convex side of the scoliosis curve. They also conducted a muscle biopsy and found predominantly type I muscle fibers in the curve convexity. ...
... The type I muscle fibers show higher fatigue resistance and lower contractile speed as opposed to the type II muscle fibers [25]. Moreover, it is also found that AIS progresses more rapidly depending on the Cobb angle, which is significantly correlated with the increased proportion of type I fibers on the convex side of the scoliotic curve [24,26]. The changes might cause the asymmetry of muscle activity. ...
... The studies also have limitations. Although many have focused on female participants since a higher percentage of patients with scoliosis are female [22][23][24], nevertheless, the gender bias inhibits the generalizability of the results. In addition, most of these studies have only focused on no more than 12 participants or even as few as 10 participants [19,20,22,24]. ...
Article
Full-text available
A large number of studies have used electromyography (EMG) to measure the paraspinal muscle activity of adolescents with idiopathic scoliosis. However, investigations on the features of these muscles are very limited even though the information is useful for evaluating the effectiveness of various types of interventions, such as scoliosis-specific exercises. The aim of this cross-sectional study is to investigate the characteristics of participants with imbalanced muscle activity and the relationships among 13 features (physical features and EMG signal value). A total of 106 participants (69% with scoliosis; 78% female; 9–30 years old) are involved in this study. Their basic profile information is obtained, and the surface EMG signals of the upper trapezius, latissimus dorsi, and erector spinae (thoracic and erector spinae) lumbar muscles are tested in the static (sitting) and dynamic (prone extension position) conditions. Then, two machine learning approaches and an importance analysis are used. About 30% of the participants in this study find that balancing their paraspinal muscle activity during sitting is challenging. The most interesting finding is that the dynamic asymmetry of the erector spinae (lumbar) group of muscles is an important (third in importance) predictor of scoliosis aside from the angle of trunk rotation and height of the subject.
... (S-EMG). Studies have reported that S-EMG activity was found to be higher on the convex side of the scoliotic curve; these findings suggest an overactivation of the paraspinal muscles as a cause of AIS [4][5][6][7] . Conversely, de Oliveira et al. reported that there was no significant difference in electromyographic amplitude of erector spinae on the convex and concave sides 8 . ...
... Conversely, de Oliveira et al. reported that there was no significant difference in electromyographic amplitude of erector spinae on the convex and concave sides 8 . These conflicting results might be due to methodological differences, based on patient selection, arbitrary focus on specific curve types or lack of controlling mechanisms to exclude inadequate posture 7,[9][10][11] . Since these studies describe conflicting results, our research attempted disaggregate analysis of the relationship between paraspinal muscle asymmetry and scoliosis curve types, considering how the curve classifications and recording levels were not accurately described in previous studies. ...
... In some studies, the authors showed that the paraspinalis muscles on the concave side have higher EMG activity, while others could not find asymmetrical activity in the paraspinalis muscles of scoliosis patients 8,9,11 . However, recent literature has reported dominance of EMG activity on the convex side of the scoliotic curve [4][5][6][7] . In this study, we measured S-EMG in a specific posture (superman position) to induce proper submaximal contraction of the paraspinalis muscles. ...
Article
Full-text available
Abstract There have been many studies on adolescent idiopathic scoliosis related abnormal muscle contractions of the spine. However, previous studies using surface electromyography to investigate paraspinal muscle asymmetry are controversial, lacking in clarity of results, and hindered by methodological limitations. The purpose of this study was to investigate the relationship between imbalance factors including surface electromyography activity according to the scoliosis curve type and leg length discrepancy and adolescent idiopathic scoliosis curve types. Seventy-nine patients with scoliosis were prospectively enrolled and were divided into five types: single thoracic, thoracolumbar, lumbar, double thoracic, and double major. Cobb angle and structural variables were measured. Surface electromyography examinations were conducted at the 7th, 12th thoracic erector spinae, 3rd lumbar erector spinae, and multifidus muscles during the superman position keeping prone spinal extension to lift the arms and legs off the floor. Whole spine radiographs were obtained to measure the Cobb angle, coronal imbalance, pelvic height and angle, and femoral head height. In the double major, thoracolumbar, and lumbar types, the mean root mean squared (RMS) EMG amplitudes were significantly higher on the convex side than the concave side (P
... Taken together, the intercellular cell communications and comparisons in GO and pathway analysis indicated that MSCs of AIS were remodeled to downregulate their osteoblast differentiation through immunocytes recruitment and interaction. Although there was a study reporting immune system abnormalities in AIS paraspinal muscle, 42,54 the present study was the first study to report the potential T lymphocyte-mediated pathogenesis, and further research is necessary to verify this hypothesis. ...
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Backgrounds Abnormal vertebral growth and development have been found in adolescent idiopathic scoliosis (AIS) patients, and the proliferation and differentiation of bone development-related cells play important roles in its pathogenesis. However, a comprehensive single-cell-level differentiation roadmap in AIS has not been achieved. Methods The present study compared the single-cell level cellular landscapes of spinal cancellous bone tissues between AIS patients and healthy subjects using high throughput single-cell RNA sequencing (scRNA-seq), which covers multiple cellular lineages including osteoblast, chondrocyte, osteoclast and related immunocytes. We constructed the differentiation trajectories of bone development-related cell lineages through pseudotime analysis, and the intercellular-communication networks between bone development-related cells and immunocytes were further developed. Results A total of 11 distinct cell clusters were identified according to the genome-wide transcriptome profiles. t-Distributed stochastic neighbor embedding (t-SNE) analysis showed that mesenchymal stem cells (MSC) were classified into three subtypes: MSC-LOXL2, MSC-IGFBP5, and MSC-GJA1. Gene ontology (GO) analysis showed that MSC-GJA1 might possess greater osteoblast differentiation potential than the others. MSC-IGFBP5 was the specific MSC subtype observed only in AIS. There were two distinct gene expression clusters: OB-DPT and OB-OLFML2B, and the counts of osteoblasts derived from AIS was significantly less than that of non-AIS subjects. In AIS patients, MSC-IGFBP5 failed to differentiate into osteoblasts and exhibited negative regulation of cell proliferation and enhanced cell death. CPC-PCNA was found to be the specific chondrocyte progenitor cell (CPC) subtype observed only in AIS patients. The cell counts of OC-BIRC3 in AIS were less than those in controls. Pseudotime analysis suggested two possible distinct osteoclast differentiation patterns in AIS and control subjects. Monocytes in AIS mainly differentiated into OC-CRISP3. Conclusions Our single-cell analysis first revealed differences existed in the cellular states between AIS patients and healthy subjects and found the differentiation disruption of specific MSC and CPC clusters in AIS. Cell communication analysis provided the possible pathogenesis of osteoblast and chondrocyte differentiation dysfunction in AIS.
... The posterior paraspinal muscles, including the multifidus and erector spinal muscle, provide dynamic stability to the spinal column [9], and its imbalance has been postulated to contribute to the initiation and/or progression of spinal deformity in AIS [10,11]. Previous studies have reported abnormal and asymmetric muscle phenotypes in concave and convex side paraspinal muscles of AIS patients, including electromyography (EMG) activities, muscle volume, muscle fiber types, and fatty and fibrosis infiltration [12][13][14][15][16]. Additionally, one recent study demonstrated a significantly lower density of activated satellite cells for fiber type I in AIS patients when compared to non-scoliosis controls, and the curve severity appeared to be associated with the density of satellite cells and other histological parameters such as cross-sectional areas of muscle fiber and myonuclear density [17]. ...
Article
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Previous studies have reported abnormal muscle morphology and functions in patients with adolescent idiopathic scoliosis (AIS). To answer whether such abnormalities could be reflected in their circulation and their clinical implication for predicting curve progression to the surgical threshold, this preliminary study explored the presence of baseline muscle-related proteins and their association with curve progression. Plasma samples were collected at the first clinical visit for AIS, with patients divided into non-progressive or progressive groups (N = four and four) according to their Cobb angle in six-year follow-ups, with age- and sex-matched healthy subjects (N = 50). Then, the samples were subjected to isobaric tags for relative and absolute quantitation (iTRAQ) for global comparison of untargeted protein expression. Seventy-one differentially expressed proteins (DEPs) were found elevated in progressive AIS. Functional analysis showed that 18 of these are expressed in muscles and play an essential role in muscle activities. Among the muscle-related DEPs, α-actin had the highest fold change in progressive/non-progressive groups. This preliminary study firstly suggested higher circulating levels of muscle structural proteins in progressive AIS, indicating the likelihood of structural damage at the microscopic level and its association with progression to the surgical threshold. Further studies with larger sample sizes are warranted to validate these novel candidates for early diagnosis and predicting progression.
... There is a hypothesis that dysfunctional paraspinal muscles may contribute the development of the scoliotic curve [2,40]. Additionally, reports have described functional and histological differences in the paraspinal muscles between the convex and the concave sides of the curve in IS patients [41,42]. ...
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The cause of adolescent idiopathic scoliosis (AIS) in humans remains obscure and probably multifactorial. At present, there is no proven method or test available to identify children or adolescent at risk of developing AIS or identify which of the affected individuals are at risk of progression. Reported associations are linked in pathogenesis rather than etiologic factors. Melatonin may play a role in the pathogenesis of scoliosis (neuroendocrine hypothesis), but at present, the data available cannot clearly show the role of melatonin in producing scoliosis in humans. The data regarding human melatonin levels are mixed at best, and the melatonin deficiency as a causative factor in the etiology of scoliosis cannot be supported. It will be an important issue of future research to investigate the role of melatonin in human biology, the clinical efficacy, and safety of melatonin under different pathological situations. Research is needed to better define the role of all factors in AIS development.
Article
Study Design. Prospective clinical electromyographic study in adolescents with idiopathic scoliosis and control group. Objective. To evaluate electromyographic amplitude from erector spinae muscles of patients with idiopathic scoliosis in comparison with control volunteers without spinal deformities. Summary of Background Data. Previous studies have indicated an increased electromyographic activity in paravertebral muscles in the convex side of the scoliotic curvature. However, in previous studies there is the absence or poor description of methods used, and some studies were conducted before the recording and processing recommendations for surface electromyographic signals had been described. Methods. Thirty individuals, matched by sex, age, and body mass index, were divided into two groups: scoliosis and control. The electric activity of the erector spinae muscles was determined by surface electromyography on both sides of the three levels of spine: T8, L2, and L5. Results. Normalized electromyographic amplitudes of erector spinae muscles, in the convex and concave sides of the apex region of the scoliotic curve in the thoracic and lumbar regions, were not significantly different. Also, there was no significant difference between the muscles of these regions when the scoliosis group was compared with the control group. The erector spinae muscle at the L5 level, representing the lower vertebral limit of the lumbar scoliotic curve, had significantly higher electromyographic activity on the convex side. However, the same alteration was shown in the control group homologous muscle (on the left side). Conclusion. Erector spinae muscles on the convex and concave sides at the curvature apex in patients with idiopathic scoliosis and small magnitude of curves did not show significant differences in electromyographic amplitude. Future studies should evaluate whether intragroup activation differences, at the L5 level in 80% of the maximum voluntary isometric contractions with predominance of the left side of the vertebral column, have any relation to the condition.