Producing effective mobility, stability, and motor control of the shoulder is a common focus of any upper extremity injury prevention or rehabilitation program. Proper static position and dynamic motion of the scapula are key components in maintaining optimal shoulder function during activity.1 A stable scapula provides a base for channeling force production through the shoulder into the upper extremity.2 Because the scapula rests on the thorax without direct structural attachment, scapular stabilization is largely dependent on the activity and coordination of the surrounding musculature. The inability to achieve proper scapular alignment and coordinated motion during activity is described as scapular dyskinesis.3 These scapular alterations may affect normal scapulohumeral rhythm, often leading to shoulder pathologies such as glenohumeral instability, labrum tears, and subacromial impingement.1,3 Identifying and acting on risk factors associated with scapular dyskinesis may aid clinicians in upper extremity injury prevention and rehabilitation.
Often overlooked as risk factors for musculoskeletal pathology in clinical practice are improper mechanics and movement patterns of ventilation. Abnormal breathing mechanics, known as breathing pattern disorders or dysfunctional breathing, have been associated with a variety of musculoskeletal dysfunctions. Breathing pattern disorders are defined as an inappropriate or inefficient method of breathing that is related to no organic cause but is persistent enough to cause symptoms.4 Individuals with breathing pattern disorders are likely to display other musculoskeletal dysfunction, such as chronic neck pain,5,6 inadequate posture,7 facial and temporomandibular joint pain,8 sacroiliac joint and back pain,9,10 and altered motor control strategies.9–11 Furthermore, several measures of breathing pattern disorders correlated to poor scores on the Functional Movement Screen system in otherwise healthy individuals.11 These findings indicate that breathing pattern disorders can be associated with the presence of various musculoskeletal impairments.
When normal and efficient inhalation occurs, the abdomen displaces anteriorly while the lower six ribs laterally expand, elevate, and rotate upward relative to the spinal column. The sternum and remainder of the thoracic cavity translate anteriorly and superiorly, increasing chest volume, as the diaphragm descends and creates a negative pressure gradient to draw air into the lungs.12 In contrast to a functional breathing pattern, which involves proper activity of the diaphragm to serve as the main driver of respiration, diaphragmic activity is reduced in a breathing pattern disorder.13 This results in a diminished negative pressure gradient inside the thoracic cavity to draw air inside the lungs. To compensate for decreased diaphragmic activity, respiratory accessory muscles become more active to superiorly translate and elevate the upper thoracic ribcage, chest, and shoulders.14 Thoracic cavity volume is then increased and air is drawn into the lungs. Breathing pattern disorders are therefore characterized by superior motion of the upper ribcage and chest that dominates over more efficient lateral and anterior expansion of the abdomen and lower ribcage.4 When this pattern of breathing occurs over time, it may become habitual and lead to functional changes in the shape of the thorax.
Many of the respiratory accessory muscles involved in breathing pattern disorders have direct or indirect attachments to the scapula and are responsible for facilitating scapular alignment and function under normal conditions. Excessive activity of the respiratory accessory muscles observed in breathing pattern disorders results in length-tension relationship and neuromuscular alterations over time.14 Research has shown altered muscular activity of many respiratory accessory muscles in individuals with scapular dyskinesis.15,16 For example, increased upper trapezius activity contributes to altered scapular upward rotation, decreased posterior tilt, and inhibition of the lower trapezius muscle to help stabilize the medial border of the scapula.15 Tightness or increased activation of the pectoralis minor may limit posterior tilting and external rotation of the scapula during dynamic arm elevation and increase scapular winging and elevation.16 Because breathing pattern disorders are related to changes in thoracic rib position and motion, as well as heightened respiratory muscle activity, it is reasonable to think that the presence of breathing pattern disorders may be accompanied by scapular dyskinesis.
The role breathing pattern disorders may have on shoulder function is not well established in current literature. Although breathing pattern disorders are thought to correlate to scapular dyskinesis within individuals4 and are related to changes in thorax position and motion during inhalation and heightened respiratory muscle activity, there is no current literature examining the relationship between the two variables using clinical assessment tools. The purpose of this study was to investigate the relationship between breathing pattern disorders and scapular dyskinesis within participants using the Manual Assessment of Respiratory Motion (MARM), Self-Evaluation of Breathing Questionnaire (SEBQ), and Scapular Dyskinesis Test (SDT). It was hypothesized that the presence of breathing pattern disorders may be accompanied by scapular dyskinesis.
A total of 45 volunteers (23 men: age = 21.35 ± 2.23 years, height = 187.53 ± 9.04 cm, mass = 95.96 ± 24.66 kg; 22 women: age = 21.77 ± 3.10 years, height = 169.60 ± 9.52 cm, mass = 63.67 ± 24.15 kg) agreed to participate in this study. All participants provided written informed consent, and the study was approved by the University of Oregon's Institutional Review Board. Participants were recruited from a local university. Thirty-two of the 45 participants were varsity athletes (14 track and field, 11 football, 4 lacrosse, 2 tennis, and 1 acrobatics and tumbling). The remaining 13 did not participate in a university varsity sport and were considered members of the general population. Forty-three of the 45 participants were right-hand dominant. Participants were included in the study if they were between the ages of 18 and 30 years, a member of the university, and able to complete four sets of five repetitions of bilateral weighted shoulder flexion and abduction through a full range of motion, as defined by the SDT.17,18 Participants were excluded if they could not complete the SDT, were currently undergoing treatment for an upper extremity musculoskeletal pathology, received breathing assistance via a medical device, or had recently received treatment for an upper extremity pathology.
The experimental protocol was approved by the University of Oregon's Institutional Review Board for the protection of human subjects. Data for all measures were collected during one 20-minute testing session at a university athletic facility. Participants filled out demographic information including sex, height, mass, age, dominant hand, sport, current injuries, and previous injuries. Data collection involved the MARM and SEBQ for the assessment of breathing pattern disorders and the SDT. The SEBQ was always performed following the MARM, so participants would not gather thoughts and opinions about their breathing while completing the SEBQ and then be focused on their breathing while performing the MARM. The testing order of the MARM and SDT was otherwise random. The primary author performed the MARM and SEBQ on all participants while a co-investigator performed the SDT on all participants for the purposes of blinding. Both investigators were certified athletic trainers.
A comprehensive evaluation of dysfunctional breathing should attempt to involve all components. Physiologically, the homeostasis of carbon dioxide within the blood is the most important factor driving respiration. Capnography is currently considered to be a valid and reliable technique in measuring this biochemical aspect of respiratory function.19,20 However, capnography is not readily accessible or feasible in the common clinical setting.
Biomechanical assessment of dysfunctional breathing is most commonly used within the clinical setting using observational skills.21 The MARM was developed to quantify the extent of thoracic breathing and other aspects of dysfunctional breathing at rest. It is of particular interest as a clinical tool because the examiner is able to derive numerical values related to the relative distribution of breathing motion and the area of breathing involvement.21 The MARM has been shown to have high levels of validity and inter-rater reliability and correlate with similar measures of respiratory induction plethysmography, which is commonly used to evaluate breathing pattern in the research setting.21–23
Breathing pattern disorders are also hypothesized to originate from a psychological or emotional source and may be part of social and behavioral patterns.21 Identifying respiratory symptoms, through self-assessment of breathing behaviors with the use of questionnaires, may be helpful in diagnosing breathing pattern disorders.24 The SEBQ was recently developed as a tool to specifically explore unexplained symptoms in individuals who experience dysfunctional breathing. The SEBQ includes various descriptions of symptoms related to dysfunctional breathing found throughout the current literature. It is a useful means of evaluating an individual's perception of his or her own breathing while possibly giving insight into the origins of the symptoms.21,25 Studies have found high test–retest reliability and internal consistency using the SEBQ and a high correlation to the earlier Nijmegen Questionnaire that was initially developed for hyperventilation syndrome.25 The SEBQ is currently the questionnaire best suited for evaluating breathing pattern disorders not associated with the presence of another respiratory disorder.21,24
Identifying scapular dyskinesis can be challenging due to the three-dimensional movement of the scapula and the surrounding musculature. Technological methods such as three-dimensional motion analysis have been developed, although these methods are not often available or feasible in the clinical setting.15,26 Several observational methods have been developed to assess scapular motion and function. The SDT was created to characterize scapular dyskinesis by the degree of its presence and pattern of abnormal motion.17,18
The MARM was performed following the protocol established by Courtney and van Dixhoorn.21 The participant was first placed in a seated position over the side of a table. The examiner sat behind the participant and placed his or her hands on the posterior and lateral aspects of the participant's lower rib cage. The examiner's hands were positioned so that the thumbs were pointing vertically and approximately parallel to the patient's spine. Fingers 4 and 5 sat below the lowest rib in a horizontal fashion so abdominal expansion could be felt. The examiner's hands were positioned comfortably on the participant as to not impede normal breathing motion but firm enough to gather a proper assessment.22 The participant was given no instruction as the examiner assessed breathing motion in the whole rib cage and abdomen, paying attention to the movement of these structures in the lateral, vertical, and anterior/posterior directions. The examiner also evaluated elevation and any shoulder shrugging, which is suggestive of upper thoracic breathing. An assessment of overall vertical motion compared to lateral motion of the lower rib cage and abdomen was made to determine whether the motion predominately arose from the upper rib cage, lower rib cage/abdomen, or a balance of the two.21
A half circle (Figure 1), divided into upper and lower halves, was used to record the examiner's interpretation. A horizontal line separated the two halves (line C). A line in the upper half was made to represent motion occurring in the upper rib cage combined with overall vertical motion (line A). A line in the lower half was made to represent motion occuring in the lower rib cage combined with the extent of lateral motion of the ribs and subtle anterior and downward movement of the abdomen caused by the inferior push of the diaphragm (line B). If there was more vertical and upper rib cage motion, the top line was drawn further from the horizontal line and closer to the top of the circle. If there was more lateral lower rib cage/abdomen motion, the bottom line was drawn further from the horizontal line and closer to the bottom of the circle. The examiner was to keep in mind the relative contribution for each upper rib cage/vertical motion and lower rib cage and abdomen/lateral motion.21
The MARM (Manual Assessment of Respiratory Motion) scoring graphic. Adapted from Courtney et al.22
The angle between lines A and C represented the extent and area of breathing movement. When breathing was deep, these two lines were recorded farther apart. If breathing was shallow, the lines were placed closer together. Balance of breathing was calculated by the difference between the angle made between lines A and C and the angle between lines B and C (angle AC minus angle BC). A value of 0 represents perfect balance of thoracic and diaphragmic breathing. A positive value indicates upper thoracic dominant breathing, whereas a negative value represents more diaphragmic dominant breathing. A value farther from 0 represents a higher presence of the respective breathing pattern.21
The SEBQ was administered following the protocol outlined by Courtney and Greenwood.25 The most current version of the SEBQ contains 25 items that are answered on a 3-point scale to reflect symptom occurrence for a maximum score of 75. Items from the SEBQ include various occurrences of breathing pattern disorders and descriptions of signs and symptoms related to dysfunctional breathing found throughout the current literature. A score of 0 = never, 1 = occasionally/a bit true, 2 = frequently/mostly true, and 3 = very frequently/very true. A higher score indicated a greater degree of dysfunctional breathing.21,24
The SDT was performed following the procedures outlined by McClure et al.17 Participants were first shown bilateral glenohumeral flexion and bilateral glenohumeral abduction movements by the examiner and then given a brief period to practice these motions. In a seated position with their arms at their side, elbows straight, and shoulders in a neutral position, participants were instructed to simultaneously elevate their arms overhead “as far as possible” to a 3-second count and then lower to a 3-second count with the thumbs pointed upward. One set of five repetitions of bilateral glenohumeral flexion was performed while the examiner observed and scored only one extremity from the posterior. This protocol was then repeated for the opposite side, then duplicated for glenohumeral abduction.17,18 The examiner recorded the findings after each repetition. Participants weighing less than 150 pounds used 3-pound dumbbells, whereas participants weighing 150 pounds or more used 5-pound dumbbells.17 Each trial of five repetitions (dominant limb flexion, dominant limb abduction, non-dominant limb flexion, and non-dominant limb abduction) was given a final rating of normal (no evidence of abnormality), subtle abnormality (mild evidence of abnormality that is not consistently present), or obvious abnormality (striking, clearly apparent abnormality and evident on at least three trials). Criteria for classifying as an abnormality included prominence of the medial, superior, or inferior border during the repetition and presence of an abnormal scapulohumeral rhythm.17 Total ratings of each extremity could then be determined using the criteria outlined in Table 1.
SDT Total Limb Score Criteria Derived From Limb Flexion and Abduction Ratings
Test–retest intra-rater reliability for the MARM and SDT was not performed. Extensive pilot testing for these two measures occurred involving a variety of participants to ensure consistency, although this was not evaluated statistically. Inter-rater reliability was a non-factor due to each measure being evaluated by only one examiner.
SPSS software (version 23.0; SPSS, Inc., Chicago, IL) was used to perform statistical bivariate correlational analysis between the variables MARM balance of breathing and SEBQ total score, MARM balance of breathing and SDT dominant limb total score, MARM balance of breathing and SDT non-dominant limb total score, SEBQ total score and SDT dominant limb total score, SEBQ total score and SDT non-dominant limb total score, and SDT dominant limb total score and SDT non-dominant limb total score. The Pearson product moment correlation coefficient (r) was calculated from each correlation with an a priori alpha level set at 0.05. Strength of correlation was defined as the following criteria from Goodwin and Leech27: r values between 1.0 and 0.5 signified a strong correlation, r values between 0.49 and 0.3 signified a moderate correlation, r values between 0.29 and 0.1 signified a weak correlation, and r values between 0.99 and 0 signified no correlation.
Descriptive statistics for all measurement variables are provided in Table 2. A significant moderate correlation was found between MARM balance of breathing and SDT non-dominant limb total score (r = 0.346, P = .020). A significant moderate correlation was found between SDT non-dominant limb total score and SDT dominant limb total score (r = 0.321, P = .032). No significant correlation was found between MARM balance of breathing and SDT dominant limb total score (r = 0.284, P = .059), although this value approached significance. No significant correlations were found between measures of MARM balance of breathing and SEBQ total score, SEBQ total score and SDT non-dominant limb total score, or SEBQ total score and SDT dominant limb total score (P ≥ .05). No significant correlations were found across different sex, sports, or injury status (P ≥ .05).
Descriptive Statistics of Assessment Methods
Breathing pattern disorders can be associated with the presence of various musculoskeletal impairments,5–11 although no research prior to our study has examined the relationship between breathing pattern disorders and scapular dyskinesis. It was hypothesized that individuals who display a degree of breathing pattern disorder would also display a similar degree of scapular dyskinesis. The primary findings indicate that there was a significant moderate correlation (r = 0.346) between MARM balance of breathing scores and SDT non-dominant limb total scores. A significant moderate correlation was found between dominant and non-dominant total limb SDT scores (r = 0.321). Interestingly, these SDT scores between limbs were only moderately correlated, although mean values and the standard deviation between dominant (2.18 ± 1.70) and non-dominant (2.00 ± 1.78) limbs were relatively similar. This finding may further enhance the notion that each limb should be given individual and independent attention in the clinical setting. No other significant differences were found between measures of breathing pattern disorders and measures of scapular dyskinesis. This study did not demonstrate a correlation between measures from the MARM and SEBQ, similar to earlier studies that failed to demonstrate significance between biomechanical and psychological measures of breathing pattern disorders.11,19
Relationship Between MARM Balance of Breathing and the SDT
The results of this study support the original hypothesis that a relationship exists between MARM balance of breathing and SDT scores, but only for the non-dominant limb. Although there has been no previous research comparing breathing pattern disorders and scapular dyskinesis, it has been hypothesized4,11 that this relationship would exist due to anatomical factors and similarities related to both conditions. It is also reasonable to think that this relationship would exist based on previous literature confirming the presence of breathing pattern disorders and other musculoskeletal conditions.5–11 However, none of this prior research has hypothesized that the non-dominant limb of an individual may be more at risk for dysfunction in the presence of a breathing pattern disorder. This finding could be related to the previously established relationship between altered motor control strategies and breathing pattern disorders.9–11 Research has indicated that non-dominant limbs may commonly display differences in neurophysiologic and biomechanical properties that influence motor control and behavior that may be detrimental.28–30 Altered neuromuscular control related to changes in muscle firing patterns and electromyography output result in scapular dyskinesis15,26; therefore, the results of this study and previous research suggest that the presence of breathing pattern disorders may coincide with the presence of scapular dyskinesis in the non-dominant limb. However, it is worth noting that on average the participants in this population displayed relatively mild scapular dyskinesis with no underlying primary pathology, such as a glenohumeral labral tear. The presence of such an injury or disorder may alter this relationship between breathing pattern disorders and scapular dyskinesis of either limb.
Relationship of SEBQ to SDT and MARM Balance of Breathing Scores
The results of this study refute the original hypothesis that breathing pattern disorders are correlated to scapular dyskinesis regarding the relationship between SEBQ and SDT scores. Participants in this study had a mean SEBQ score of 13.02 ± 7.12. Normative values for the SEBQ have not been established, although two studies have previously found mean SEBQ scores of 1319 and 1625 in a population that had concerns about their breathing and reported symptoms of breathing difficulties. This suggests that the population in the current study may, on average, display mild breathing pattern disorders according to the SEBQ, but their scores may not be severe enough to demonstrate a true breathing pattern disorder.
Previous studies failed to find a correlation between the psychological evaluation of breathing pattern disorders and the presence of musculoskeletal conditions,11 although the amount of research performed on this topic is limited. No correlation was observed between the SEBQ and MARM balance of breathing scores in the current study. Prior research has shown mixed results in finding a correlation between survey-based psychological breathing pattern disorders measures and biomechanical breathing pattern disorders measures.11,19,25,31 It is important to keep in mind that the SEBQ only represents one aspect of multi-dimensional breathing pattern disorders and is meant to provide one piece of the overall examination of breathing pattern disorders. For this reason, it has been recommended to include a biomechanical, physiological, and psychological measurement when evaluating breathing pattern disorders.19
Limitations and Suggestions for Future Research
A major limitation of the current study was the subjective nature of the involved assessments. Although these are the types of assessments that are going to be used in the clinical setting, including a “gold standard” measurement such as capnography or three-dimensional motion analysis for comparison may have been helpful. The inability to distinguish breathing pattern differences between left and right sides using the MARM to compare with left and right SDT measures was a limitation of this study. It is also unknown whether the participants had previously been instructed on proper scapular cueing during overhead motions, leading to potential false-negative results.
Furthermore, shape of the distributions of the MARM balance of breathing scores and SDT scores were grossly uneven, which effects the correlational analysis. The maximum value of a correlation decreases as the difference between each variable's distribution increases.27 MARM balance of breathing scores had a range of 44, whereas SDT total limb scores had a range of 6; therefore, the strength of the correlations found between these two measures may have been negatively affected. Although a standard “yes/no” scoring system is used in the SDT in the literature,1,17 it is not believed that the use of such criteria in the current study would avoid limitation. This is due primarily to the fact that participants in the current study demonstrated only mild to moderate scapular dyskinesis with no underlying primary glenohumeral pathology.
Future research including objective measures, such as capnography and three-dimensional motion analysis, is warranted for the purposes of assessing reliability and comparison to subjective measures. Adding these additional clinical breathing assessments may also be helpful in fully diagnosing breathing pattern disorders. A next step for future research is to assess the effects of a proper breathing pattern-based intervention on the effects of scapular kinesis or shoulder pain within participants who present with scapular dyskinesis.
Implications for Clinical Practice
Our results indicate that breathing pattern disorders may be related to scapular dyskinesis of the non-dominant limb, further reinforcing the opinion that clinicians need to treat patients bilaterally. The current study also suggests that the lay practitioner may be able to find a relationship between breathing pattern disorders and scapular dyskinesis in a typical clinical setting while using no equipment. Upper extremity pathologies account for a large portion of physical ailments and may have a significant impact on athletic function, activities of daily living, and quality of life. Focusing on breathing pattern during rehabilitation or prevention of upper extremity injuries, in addition to common practices such as strength and scapular stability, may result in better outcomes.
- Uhl TL, Kibler WB, Gecewich B, Tripp BL. Evaluation of clinical assessment methods for scapular dyskinesis. Arthroscopy. 2009;25:1240–1248. doi:10.1016/j.arthro.2009.06.007 [CrossRef]
- Struyf F, Cagnie B, Cools A, et al. Scapulothoracic muscle activity and recruitment timing in patients with shoulder impingement symptoms and glenohumeral instability. J Electromyogr Kinesiol. 2014;24:277–284. doi:10.1016/j.jelekin.2013.12.002 [CrossRef]
- Ludewig PM, Cook TM. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther. 2000;80:276–291.
- Clifton-Smith T, Rowley J. Breathing pattern disorders and physiotherapy: inspiration for our profession. Physical Therapy Reviews. 2011;16:75–86. doi:10.1179/1743288X10Y.0000000025 [CrossRef]
- Kapreli E, Vourazanis E, Billis E, Oldham JA, Strimpakos N. Respiratory dysfunction in chronic neck pain patients: a pilot study. Cephalalgia. 2009;29:701–710. doi:10.1111/j.1468-2982.2008.01787.x [CrossRef]
- Perri MA, Halford E. Pain and faulty breathing: a pilot study. Journal of Bodywork and Movement Therapies. 2004;8:297–306. doi:10.1016/S1360-8592(03)00085-8 [CrossRef]
- Lewit K. Relation of faulty respiration to posture, with clinical implications. J Am Osteopath Assoc. 1980;79:525–529.
- Hruska RJ Jr, . Influences of dysfunctional respiratory mechanics on orofacial pain. Dent Clin North Am. 1997;41:211–227.
- O'Sullivan PB, Beales DJ, Beetham JA, et al. Altered motor control strategies in subjects with sacroiliac joint pain during the active straight-leg-raise test. Spine (Phila Pa 1976). 2002;27:E1–E8. doi:10.1097/00007632-200201010-00015 [CrossRef]
- Grimstone SK, Hodges PW. Impaired postural compensation for respiration in people with recurrent low back pain. Exp Brain Res. 2003;151:218–224. doi:10.1007/s00221-003-1433-5 [CrossRef]
- Bradley H, Esformes J. Breathing pattern disorders and functional movement. Int J Sports Phys Ther. 2014;9:28–39.
- De Troyer A, Estenne M. Functional anatomy of the respiratory muscles. Clin Chest Med. 1988;9:175–193.
- Courtney R. The functions of breathing and its dysfunctions and their relationship to breathing therapy. International Journal of Osteopathic Medicine. 2009;12:78–85. doi:10.1016/j.ijosm.2009.04.002 [CrossRef]
- Kolar P, Kobesova A, Valouchova P, Bitnar P. Dynamic neuromuscular stabilization: Developmental kinesiology: breathing stereotypes and postural-locomotion function. In: Chaitow L, Bradley D, Gilbert C. Recognizing and Treating Breathing Disorders: A Multi-disciplinary Approach, 2nd ed. Philadelphia: Elsevier; 2014:11–22. doi:10.1016/B978-0-7020-4980-4.00002-2 [CrossRef]
- Huang TS, Ou HL, Huang CY, Lin JJ. Specific kinematics and associated muscle activation in individuals with scapular dyskinesis. J Shoulder Elbow Surg. 2015:24:1227–1234. doi:10.1016/j.jse.2014.12.022 [CrossRef]
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- Courtney R, van Dixhoorn J. Questionnaires and manual methods for assessing breathing dysfunction. In: Chaitow L, Bradley D, Gilbert C. Recognizing and Treating Breathing Disorders: A Multi-disciplinary Approach, 2nd ed. Philadelphia: Elsevier; 2014:137–146. doi:10.1016/B978-0-7020-4980-4.00012-5 [CrossRef]
- Courtney R, Cohen M, Reece J. Comparison of the manual assessment of respiratory motion (MARM) and the hi lo breathing assessment in determining a simulated breathing pattern. International Journal of Osteopathic Medicine. 2009;12:86–91. doi:10.1016/j.ijosm.2008.10.002 [CrossRef]
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SDT Total Limb Score Criteria Derived From Limb Flexion and Abduction Ratings
|SDT Total Score||Description|
|0||Both flexion and abduction movements rated as normal|
|1||One movement rated as normal, one movement rated as subtle|
|2||Both flexion and abduction movements rated as subtle|
|3||One movement rated as normal, one movement rated as obvious|
|4||One movement rated as subtle, one movement rated as obvious|
|5||Both flexion and abduction movements rated as obvious|
Descriptive Statistics of Assessment Methods
|MARM balance of breathing||−3||40||13.87||10.50|
|SEBQ total score||2||28||13.02||7.12|
|SDT dominant limb total score||0||5||2.18||1.70|
|SDT non-dominant total score||0||5||2.00||1.78|