Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation

Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation

Journal of Biomechanics xxx (2017) xxx–xxx Contents lists available at ScienceDirect Journal of Biomechanics journal homepage: www.elsevier.com/loca...

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Journal of Biomechanics xxx (2017) xxx–xxx

Contents lists available at ScienceDirect

Journal of Biomechanics journal homepage: www.elsevier.com/locate/jbiomech www.JBiomech.com

Scapular kinematics in adolescent idiopathic scoliosis: A threedimensional motion analysis during multiplanar humeral elevation Elif Turgut a,⇑, Gozde Gur a, Cigdem Ayhan a, Yavuz Yakut a,c, Gul Baltaci b a

Hacettepe University, Faculty of Health Sciences, Department of Physiotherapy and Rehabilitation, Ankara, Turkey Private Guven Hospital, Ankara, Turkey c Hasan Kalyoncu University, Department of Physiotherapy and Rehabilitation, Gaziantep, Turkey b

a r t i c l e

i n f o

Article history: Accepted 22 July 2017 Available online xxxx Keywords: Scapula Posture Kinematics Scoliosis Adolescent Idiopathic

a b s t r a c t The scapula plays a critical role in supporting shoulder function. Considering the closed anatomical relationship between the scapula and the thoracic cage, the presence of postural disturbances could be linked to alterations in the scapular position and orientation in adolescent idiopathic scoliosis (AIS). However, currently there is a lack of descriptive research and detailed assessment of scapular kinematics in AIS. The aim of this study was to investigate the three-dimensional scapular kinematics in AIS. Nineteen AIS patients and fourteen healthy controls participated in this study. Bilateral shoulder kinematics were measured with an electromagnetic tracking device during shoulder elevation in the sagittal, scapular, and frontal planes. Data for the scapular orientation were analyzed in the resting position and at 30°, 60°, 90°, and 120° of humerothoracic elevation. Scapular behavior was different in participants with AIS, compared to healthy controls, with different patterns observed on convex and concave sides. While examining all three planes of elevation, the scapula was more internally and anteriorly tilted on the convex side, while the scapula was more externally, downwardly rotated, and posteriorly tilted on the concave side in participants with AIS. Furthermore, there was a decreased peak humerothoracic elevation and altered scapular posterior tilt in participants with AIS in the resting position. These findings increase our knowledge and understanding of scapular alterations and the reported scapular alterations can be considered as adaptive compensation strategies in AIS. Ó 2017 Elsevier Ltd. All rights reserved.

1. Introduction Shoulder elevation is a complex motion that occurs because of combined humerus, clavicle, spine, and scapula movement (Inman et al., 1996; Theodoridis and Ruston, 2002). The scapula plays a critical role in supporting a wide range of glenohumeral motions and normal shoulder function (Kibler, 1998). Alterations in scapular kinematics are often related to various shoulder disorders (Ludewig and Reynolds, 2009). Common causes including postural problems, dysfunction of the scapular muscular force couples, and flexibility deficits of the pectoralis minor and posterior capsule may affect scapulohumeral motion (Ludewig and Reynolds, 2009). Adolescent idiopathic scoliosis (AIS) is a structural, lateral, rotated curvature of the spine that arises in otherwise healthy

⇑ Corresponding author at: Hacettepe University, Faculty of Health Sciences, Department of Physiotherapy and Rehabilitation, 06100 Samanpazari, Ankara, Turkey. E-mail address: [email protected] (E. Turgut).

children at or around puberty (Weinstein et al., 2008). This spinal deformity is characterized by a curved spine and is usually accompanied by geometric and morphologic changes in the trunk and thoracic cage deformity (LeBlanc et al., 1997; Stokes, 1994). Despite decades of intensive research, the cause and pathophysiology of AIS is not well understood; however, many factors have been associated with AIS including central nervous system alteration (Adler et al., 1986; Herman et al., 1985; Keessen et al., 1992; Sahlstrand et al., 1978), sensory-motor deficits (Barrack et al., 1988; Keessen et al., 1992; Wyatt et al., 1986), and impaired static and dynamic neuromuscular control (Beaulieu et al., 2009; Byl and Gray, 1993; Lao et al., 2008; Nault et al., 2002). The spinal deformity not only modifies the shape of the trunk but also changes relations between body segments (Goldberg et al., 2001; Samuelsson and Noren, 1997; Stokes, 1994). Considering the closed anatomical relationship between the scapula and the thoracic cage, the presence of the aforementioned factors could be linked to alterations in the scapular position and orientation in AIS. Altered proximal orientation may further affect shoulder and upper extremity function and lead to altered force transfer.

http://dx.doi.org/10.1016/j.jbiomech.2017.07.029 0021-9290/Ó 2017 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Turgut, E., et al. Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation. J. Biomech. (2017), http://dx.doi.org/10.1016/j.jbiomech.2017.07.029

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E. Turgut et al. / Journal of Biomechanics xxx (2017) xxx–xxx

Upper limb dysfunction such as lower levels of self-reported shoulder function (Lin et al., 2010), decreased grip strength (Martinez-Liorens et al., 2010), proprioceptive deficit (Keessen et al., 1992) and shoulder pain (Grubb and Lipscomb, 1992) were previously reported especially for adult scoliosis. Lin et al. (2010) investigated resting and scapular plane elevation kinematics and reported alterations in scapular orientation in the resting position when comparing idiopathic scoliosis in adolescents and adults with healthy controls. However, younger populations have different scapular behavior compared with adults (Dayanidhi et al., 2005). There is a lack of descriptive research and detailed assessment of scapular kinematics in AIS. Investigating threedimensional (3D) scapular kinematics during shoulder elevation in different movement planes may therefore enhance the field’s knowledge regarding scapular behavior in AIS and help advance our understanding of the patterns and magnitude of scapulothoracic movement adaptations in this population. Accordingly, we aimed to investigate 3D scapular kinematics in AIS. We hypothesized that the convex and concave shoulder side of participants with AIS would have alterations in scapular kinematics during multiplanar humeral elevation and scapular orientation in the resting position, when compared with the dominant and nondominant side of healthy controls. 2. Materials and methods 2.1. Participants A total of thirty-three pain-free participants with AIS (n = 19) and healthy controls (n = 14) were recruited in the study (Table 1). Inclusion criteria for participants with AIS consisted of a right thoracic left lumbar double curve pattern scoliosis with a primary thoracic curve Cobb angle between 20° and 45°. Cobb angle was measured using standard antero-posterior radiographs in a standing position. Participants with AIS also had no history of shoulder pain, no prior intervention, and had arm dominance on their convex side. Healthy controls were selected from asymptomatic volunteers who had no history of shoulder pain or injury related to the upper body and extremities. Participants were excluded if they had any known systemic or neurological disorders including cervical radiculopathy, performed repetitive overhead shoulder movements related to occupation or sports activities on a regular basis, or had a body mass index >30 kg/m2. The Institutional Research Ethics Board approved the protocol for this study and all participants signed informed consent forms. 2.2. Instrumentation

Table 1 Characteristics of participants.

Cobb Angle (degrees) ASES Score (points)

2.3. Experimental procedure First, five sensors were attached directly to the skin over flattest aspect of the each acromion, postero-lateral aspect of the each humerus distal to triceps belly and T1 thoracic vertebrae with double-sided adhesive tape and further secured with nonelastic tape. Second, specific bony landmarks were digitized with a stylus based on International Society of Biomechanics standard protocol while participants were standing with their arms relaxed (Wu et al., 2005). Third, the data analysis were performed and further described using the Euler angle sequence (Ayhan et al., 2015; Turgut et al., 2016). Scapular orientation in the resting position was recorded bilaterally; kinematic data were collected for 5 s in the patient’s resting standing posture with arms relaxed at the sides. Sagittal plane, scapular plane, and frontal plane elevation were assessed. Scapular plane was oriented 40° anterior to the coronal plane (Borstad and Ludewig, 2005). Participants performed three repetitions of bilateral, full overhead arm elevation in three movement planes, using the wooden poles as a guide, at a speed matching the beat of a metronome set at 60 beats per minute, using 3 s for elevation. Prior to recording, each participant performed a series of elevation in the specific movement plane to warm-up and to familiarize. Thirty seconds were provided between recordings to avoid fatigue. Additionally, during kinematic recordings, verbal comments were made to achieve full elevation. The order of the movement plane was randomized using random numbers generated by a computer. Data for scapular orientation at 30°, 60°, 90°, and 120° of humerothoracic elevation were obtained for each repetition. The y-x0 -z00 sequence was used to define scapular rotations; the first rotation defined the amount of internal-external rotation, second upward-downward rotation, and last anterior-posterior tilt. The scapular orientation values at rest, at each angle of humerothoracic elevation, and peak humerothoracic elevation angles for each movement were averaged across the three repetitions. Data collected with this electromagnetic tracking system are reliable, with calculated between-day ICC values ranging from 0.70 to 0.82; standard error of measurement values ranging from 3.37° to 6.79° for scapular kinematics (Haik et al., 2014). This method of measuring 3D scapular kinematics has previously been validated below 120° of elevation (Karduna et al., 2001). 2.4. Statistical analysis

3 D kinematic data for the scapula were collected with a Flock of Birds electromagnetic tracking system (Ascension Technology

Age (years) Height (m) Weight (kg) Gender (n)

Corporation, Shelburne, VT, USA). This system interfaced with the Motion Monitor software program (Innovative Sports Training Inc., Chicago, IL, USA).

Participants with AIS n = 19

Healthy controls n = 14

p

13.8 (1.9) 157.7 (11.1) 46.2 (9.4) 17 Female 2 Male 32.6 (7.9) 96.1 (2.6)

13.7 (2) 159.7 (8.3) 50.1 (7.8) 11 Female 3 Male N/A 97.4 (1.8)

0.93 0.57 0.22 0.38 N/A 0.12

Note: Data given as mean and standard deviation (for age, height, weight and Cobb angle), or as counted numbers (gender). AIS; Adolescent idiopathic scoliosis, ASES; American Shoulder and Elbow Surgeons. Exact p values based on student-t test for age, height, and weight; and Fisher’s exact test for gender.

Sample size was determined based on a pilot study with nine patients using a power of 0.80 and / = 0.05. Using the primary outcome variable of scapular upward rotation, it was determined that 14 participants were required in each group. The assumption of normality was tested prior to statistical analysis by inspecting skewness and kurtosis. Statistical analysis of kinematic data was then performed using two separate two-way ANOVAs (group-byangle) for each scapular movement obtained during sagittal, scapular and frontal plane elevations; with the group set as the betweensubjects factor and the angle (30°, 60°, 90°, and 120° humerothoracic elevation) set as the repeated factor. One ANOVA was used to compare scapular rotations between the convex side of participants with AIS to the dominant side of healthy controls, and one was used to compare the concave side of participants with AIS to the nondominant side of healthy controls. When an interaction term was significant, pairwise analyses were performed using a Bonferroni adjustment. The examination of post-hoc results was

Please cite this article in press as: Turgut, E., et al. Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation. J. Biomech. (2017), http://dx.doi.org/10.1016/j.jbiomech.2017.07.029

E. Turgut et al. / Journal of Biomechanics xxx (2017) xxx–xxx

limited to between-group comparisons. When an interaction term was insignificant, the main effect for the group was evaluated. Greenhouse–Geisser correction was used to adjust the degrees of freedom when the sphericity assumption was violated. Comparison of scapular orientation obtained in the resting position and peak humerothoracic elevation was performed using an independent-samples Student’s t-test to compare groups. Effect Size (ES) and minimal important difference (MID) were calculated

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to evaluate clinical relevance (Armijo-Olivo et al., 2011). The alpha level for determining statistical significance was set at 0.05. 3. Results In general, the scapula moved toward internal rotation or external rotation, upward rotation, and posterior tilt during shoulder elevation for all participants (Figs. 1–3, Table 2).

Fig. 1. Scapular kinematics during shoulder elevation in the sagittal plane among participants with adolescent idiopathic scoliosis and healthy controls. Note: Data are presented as Mean and Standard Deviation. AIS; Adolescent idiopathic scoliosis. *Significant pairwise comparisons between the convex side of participants with AIS and the dominant side of healthy controls at this angle (p < 0.05). §Significant pairwise comparisons between the concave side of participants with AIS and the nondominant side of healthy controls at this angle (p < 0.05).

Fig. 2. Scapular kinematics during shoulder elevation in the scapular plane among participants with adolescent idiopathic scoliosis and healthy controls. Note: Data are presented as Mean and Standard Deviation. AIS; Adolescent idiopathic scoliosis. *Significant pairwise comparisons between the convex side of participants with AIS and the dominant side of healthy controls at this angle (p < 0.05). §Significant pairwise comparisons between the concave side of participants with AIS and the nondominant side of healthy controls at this angle (p < 0.05).

Fig. 3. Scapular kinematics during shoulder elevation in the frontal plane among participants with adolescent idiopathic scoliosis and healthy controls. Note: Data are presented as Mean and Standard Deviation. AIS; Adolescent idiopathic scoliosis. *Significant pairwise comparisons between the convex side of participants with AIS and the dominant side of healthy controls at this angle (p < 0.05). §Significant pairwise comparisons between the concave side of participants with AIS and the nondominant side of healthy controls at this angle (p < 0.05).

Please cite this article in press as: Turgut, E., et al. Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation. J. Biomech. (2017), http://dx.doi.org/10.1016/j.jbiomech.2017.07.029

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E. Turgut et al. / Journal of Biomechanics xxx (2017) xxx–xxx

Table 2 Scapular kinematics for participants with AIS and healthy controls. Scapular kinematics Sagittal plane Internal/external rotation

HT elevation level

AIS Mean (SD) degrees

Healthy controls Mean (SD) degrees

Convex/dominant side Convex/dominant side Convex/dominant side Convex/dominant side Concave/nondominant Concave/nondominant Concave/nondominant Concave/nondominant Convex/dominant side Convex/dominant side Convex/dominant side Convex/dominant side Concave/nondominant Concave/nondominant Concave/nondominant Concave/nondominant Convex/dominant side Convex/dominant side Convex/dominant side Convex/dominant side Concave/nondominant Concave/nondominant Concave/nondominant Concave/nondominant

30° 60° 90° 120° side 30° side 60°* side 90°* side 120°* 30° 60° 90° 120° side 30° side 60° side 90°* side 120°* 30° 60° 90° 120° side 30° side 60° side 90° side 120°

39.6 (7.6) 42.7 (8.2) 44.1 (8.1) 41.3 (9.6) 29.2 (7.7) 31.8 (9.5) 32.7 (10.5) 25.9 (12.3) 1.4 (6.1) 11.6 (9) 18.1 (9) 23.7 (9.8) 2.2 (8.5) 9.1 (10.6) 14.4 (11.8) 16.9 (13.4) 12.6 (8.2) 13.8 (12.3) 12.5 (15.2) 11.2 (16.7) 5.1 (9.5) 5.4 (12.8) 4.2 (15) 1.8 (15.8)

36.6 (4.3) 42.6 (4.9) 45.2 (5.2) 42.1 (7.1) 33.7 (6.1) 40.1 (7.7) 43.8 (9.2) 39.8 (9.1) 0.9 (6.1) 7.9 (7) 17.8 (8.3) 26.8 (9.8) 2.3 (4.8) 12.2 (5) 22.9 (6.2) 32.4 (8.2) 10.6 (4.3) 11.1 (4.3) 9.9 (5.4) 4.2 (5.9) 10.6 (3.7) 11.2 (4.4) 10.3 (4.3) 5.2 (6.7)

Convex/dominant side Convex/dominant side Convex/dominant side Convex/dominant side Concave/nondominant Concave/nondominant Concave/nondominant Concave/nondominant

30° 60° 90° 120° side 30° side 60° side 90° side 120°

34.4 (9.8) 36.7 (9.3) 39.3 (9.1) 41.2 (11.5) 24.5 (7.1) 35.6 (9.7) 28.5 (10.5) 27 (14.1)

29.3 (5.9) 31.7 (7.7) 33.8 (8.6) 35.1 (9) 24.9 (5.9) 28.5 (7.5) 31 (7.7) 31.7 (8.6)

Upward/downward rotation

Convex/dominant side Convex/dominant side Convex/dominant side Convex/dominant side Concave/nondominant Concave/nondominant Concave/nondominant Concave/nondominant

30° 60° 90° 120° side 30° side 60° side 90°* side 120°*

0.4 (7.1) 8.6 (7.4) 15.5 (7.6) 23.1 (8.7) 0.5 (7.7) 6.5 (9.4) 12.9 (11) 16.5 (13.4)

1.1 (4.9) 8.1 (5.5) 17.1 (6.7) 25.6 (9.1) 1.5 (3.9) 11.1 (4.2) 20.8 (5.4) 32 (9.2)

Anterior/posterior tilt

Convex/dominant side Convex/dominant side Convex/dominant side Convex/dominant side Concave/nondominant Concave/nondominant Concave/nondominant Concave/nondominant

30° 60° 90° 120°* side 30° side 60° side 90° side 120°

13.6 (9.2) 13.6 (11.3) 12.7 (13.9) 13.7 (16.1) 6.5 (9.3) 6.8 (11) 5.3 (12.8) 3.1 (15.1)

11.8 (5) 10.9 (4.9) 9 (5.1) 4.8 (4.8) 11.1 (4.2) 10.3 (5.1) 7.7 (5.2) 3.7 (5.5)

Convex/dominant side Convex/dominant side Convex/dominant side Convex/dominant side Concave/nondominant Concave/nondominant Concave/nondominant Concave/nondominant

30°** 60°** 90°** 120°** side 30°** side 60°** side 90°** side 120°**

28.7 28.2 30.4 35.6 19.1 17.9 20.2 23.7

20.6 18.8 28.3 23.1 28.1 26.6 30.7 33.3

Upward/downward rotation

Convex/dominant side Convex/dominant side Convex/dominant side Convex/dominant side Concave/nondominant Concave/nondominant Concave/nondominant Concave/nondominant

30° 60° 90° 120° side 30° side 60°* side 90°* side 120°*

1.4 (5.8) 7.4 (6.4) 15 (7.7) 21.9 (10) 3.4 (8.7) 4.2 (10.7) 10.3 (10.7) 14.5 (11.3)

1.6 (5.6) 8.2 (6.7) 19 (8.6) 28.7 (11.1) 1.5 (5.6) 11.7 (5.2) 23.7 (8.4) 35 (10.2)

Anterior/posterior tilt

Convex/dominant Convex/dominant Convex/dominant Convex/dominant

30° 60° 90°* 120°*

16.4 14.9 14.1 15.7

11.5 (5) 8.6 (5.5) 4.4 (6.8) 2.6 (6.6)

Upward/downward rotation

Anterior/posterior tilt

Scapular plane Internal/external rotation

Frontal plane Internal/external rotation

side side side side

(11.2) (13.4) (13.1) (12.3) (9.6) (12.9) (12.9) (12.1)

(9.2) (11.9) (13.2) (15.8)

(7.2) (8.5) (9.5) (11.4) (8.6) (6.9) (8.4) (7.4)

Please cite this article in press as: Turgut, E., et al. Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation. J. Biomech. (2017), http://dx.doi.org/10.1016/j.jbiomech.2017.07.029

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E. Turgut et al. / Journal of Biomechanics xxx (2017) xxx–xxx Table 2 (continued) Scapular kinematics

HT elevation level Concave/nondominant Concave/nondominant Concave/nondominant Concave/nondominant

side side side side

30° 60° 90° 120°

AIS Mean (SD) degrees

Healthy controls Mean (SD) degrees

8.9 7.2 6.2 6.2

11.4 (3.8) 8.4 (4.7) 3.7 (4.2) 1.1 (5.2)

(9.2) (12.9) (14.3) (15.1)

Note. AIS, Adolescents Idiopathic Scoliosis; HT, humerothoracic elevation; SD, standard deviation. * Indicates statistically significant pairwise comparisons. ** Indicates statistically significant main effect.

3.1. Scapular orientation; convex side of participants with AIS versus dominant side of healthy controls 3.1.1. Sagittal plane There was no statistically significant group-by-angle interaction or main effect for scapular internal-external rotation (p > 0.05). There was a statistically significant group-by-angle interaction for scapular upward-downward rotation (F1.8,55.8 = 3.3, p = 0.04). Despite this significant interaction, pairwise comparisons for each of the four angles of elevation failed to indicate any significant differences between groups at any of the angles (Fig. 1). There was no statistically significant group-by-angle interaction or main effect for scapular anterior-posterior tilt (p > 0.05). 3.1.2. Scapular plane There was no statistically significant group-by-angle interaction or main effect for scapular internal-external rotation and for scapular upward-downward rotation (p > 0.05). There was a statistically significant group-by-angle interaction for scapular anteriorposterior tilt (F1.2,37.3 = 6.31, p = 0.01). Pairwise comparisons indicated that the scapula was more anteriorly tilted on the convex side of participants with AIS at scapular plane elevation angles of 120° (p = 0.04; mean difference, 8.9°; ES, 0.7; MID, 2.5° and 6.3°; Fig. 2). 3.1.3. Frontal plane There was no statistically significant group-by-angle interaction (F1.6,50.5 = 2.69, p = 0.08) for scapular internal-external rotation. However, there was a main effect (F1,31 = 7.606, p = 0.01; 30.7° for convex side of participants with AIS versus 20.2° for dominant side of healthy controls; ES, 0.97; MID, 2.1° and 5.4°) of group for scapular internal-external rotation indicating that the amount of scapular internal rotation during frontal plane elevation was greater in the AIS group than in the healthy controls (Fig. 3). There was a statistically significant group-by-angle interaction for scapular upward-downward rotation (F1.2,37.9 = 4.34, p = 0.03). Despite this significant interaction, pairwise comparisons for each of the four angles of elevation failed to indicate any significant differences between groups at any of the angles (Fig. 3). There was a statistically significant group-by-angle interaction for scapular anterior-posterior tilt (F1.2,38.9 = 8.15, p = 0.004). Pairwise comparisons indicated that the scapula was more anteriorly tilted on the convex side of participants with AIS at frontal plane elevation angles of 90° (p = 0.01; mean difference, 9.7°; ES, 0.88; MID, 2.2° and 5.5°) and 120° (p = 0.007; mean difference, 13.1°; ES, 1.02; MID, 2.5° and 6.4°; Fig. 3). 3.2. Scapular orientation; concave side of participants with AIS versus nondominant side of healthy controls 3.2.1. Sagittal plane There was a statistically significant group-by-angle interaction (F1.6,49.7 = 8.05, p = 0.002) for scapular internal-external rotation. Pairwise comparisons indicated that the scapula was more exter-

nally rotated on the concave side of participants with AIS at sagittal plane elevation elevation angles of 60° (p = 0.01; mean difference, 8.3°; ES, 0.93; MID, 1.7° and 4.4°), 90° (p = 0.004; mean difference, 11.1°; ES, 1.1; MID, 2° and 5°), and 120° (p = 0.001; mean difference, 13.9°; ES, 1.2; 2.2° and 5.5°; Fig. 1). There was statistically a significant group-by-angle interaction for scapular upwarddownward rotation (F1.6,52.2 = 22.35, p < 0.001). Pairwise comparisons indicated that the scapula was more downwardly rotated on the concave side of participants with AIS at sagittal plane elevation elevation angles of 90° (p = 0.01; mean difference, 8.5°; ES, 0.85; MID, 1.9° and 4.9°) and 120° (p = 0.001; mean difference, 15.5°; ES, 1.3; MID, 2.3° and 5.7°; Fig. 1). There was no statistically significant group-by-angle interaction or main effect for scapular anterior-posterior tilt (p > 0.05). 3.2.2. Scapular plane There was no statistically significant group-by-angle interaction or main effect for scapular internal-external rotation and for scapular anterior-posterior tilt (p > 0.05). There was a statistically significant group-by-angle interaction for scapular upward-downward rotation (F1.4,44.1 = 15.17, p < 0.001). Pairwise comparisons indicated that the scapula was more downwardly rotated on the concave side of participants with AIS at scapular plane elevation angles of 90° (p = 0.01; mean difference, 7.9°; ES, 0.86; 1.8° and 4.5°) and 120° (p = 0.001; mean difference, 15.5°; ES, 1.3; MID 2.3° and 5.9°; Fig. 2). 3.2.3. Frontal plane There was no statistically significant group-by-angle interaction (F2.1,65.4 = 0.16, p = 0.85) for scapular internal-external rotation. However, there was a main effect (F1, 31 = 8.45, p = 0.007; 20.2° for concave side of participants with AIS versus 29.7° for nondominant side of healthy controls; ES, 1.02; MID, 1.8° and 4.5°) of group for scapular internal-external rotation indicating that the amount of scapular external rotation during frontal plane elevation was greater in the AIS group than in the healthy controls (Fig. 3). There was a statistically significant group-by-angle interaction for scapular upward-downward rotation (F1.5,47.2 = 28.14, p < 0.001). Pairwise comparisons indicated that the scapula was more downwardly rotated on the concave side of participants with AIS at 60° frontal plane elevation angles of (p = 0.02; mean difference, 7.5°; ES, 0.84; MID, 1.7° and 4.4°), 90° (p = 0.001; mean difference, 13.4°; ES, 1.3; MID, 1.9° and 4.9°), and 120° (p < 0.001; mean difference, 20.5°; ES, 1.8; 2.1° and 5.4°; Fig. 3). There was a statistically significant group-by-angle interaction for scapular upwarddownward rotation (F1.4,44.5 = 7.54, p = 0.004). Despite this significant interaction, pairwise comparisons for each of the four angles of elevation failed to indicate any significant differences between groups at any of the angles (Fig. 3). 3.3. Peak humerothoracic elevation Comparisons of peak humerothoracic elevation between participants with AIS and healthy controls indicated that there was less

Please cite this article in press as: Turgut, E., et al. Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation. J. Biomech. (2017), http://dx.doi.org/10.1016/j.jbiomech.2017.07.029

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humerothoracic elevation achieved during sagittal plane elevation (p = 0.03; mean difference, 12.9°; ES, 1.3; MID, 1.8° and 4.5°), scapular plane (p < 0.001; mean difference, 14.4°; ES, 1.5; MID, 1.9° and 4.7°), and frontal plane elevation (p = 0.001; mean difference, 13.2°; ES, 1.2; MID, 2.1° and 5.1°) on the convex side of participants with AIS; and there was less humerothoracic elevation achieved during sagittal plane elevation (p = 0.03; mean difference, 7.2°; ES, 0.74; MID, 1.9° and 4.8°), scapular plane (p = 0.008; mean difference, 8.9°; ES, 0.99; MID, 1.7° and 4.4°), and frontal plane elevation (p = 0.002; mean difference, 10.7°; ES, 1.19; MID, 1.7° and 4.4°) on the concave side of participants with AIS (Fig. 4, Table 3). 3.4. Resting position Comparisons of scapular orientation in resting position between participants with AIS and healthy controls indicated that the scapula was more posteriorly tilted on the concave side of par-

Fig. 4. Peak humerothoracic elevation angle during shoulder elevation in the sagittal, scapular, and frontal planes among participants with adolescent idiopathic scoliosis and healthy controls. Note: Data are presented as Mean and Standard Deviation. AIS; Adolescent idiopathic scoliosis. *Significant pairwise comparisons between groups (p < 0.05).

ticipants with AIS (p = 0.002; mean difference, 7.6°; ES, 1.14; MID, 1.3° and 3.3°; Fig. 5). There were no differences found for other scapular rotations in the resting position (p > 0.05).

4. Discussion This study provides new information describing the scapular kinematic alterations in participants with AIS. We found that the scapula was more internally, downwardly rotated, and anteriorly tilted on the convex side, and more externally, downwardly rotated, and posteriorly tilted on the concave side in participants with AIS when compared to healthy controls. Additionally, decreased peak humerothoracic elevation and altered scapular posterior tilt on concave side in the resting position were observed in participants with AIS. There are several potential mechanisms that may result in shoulder kinematic alterations, including postural disturbances, altered scapular muscle activation, and soft tissue tightness (Lin et al., 2010; Ludewig and Reynolds, 2009). From a mechanical perspective, a pattern of kinematic differences followed postural distortions and misalignment of the trunk and the scapular disorientation could not be compensated at specific endpoints throughout a range of motion. Our findings showed that the scapular kinematic differences between study groups reached 20° for upward rotation during elevation and all of the differences were clinically relevant when considering ES and MID calculations

Fig. 5. Scapular kinematics in resting position among participants with adolescent idiopathic scoliosis and healthy controls. Note: Data are presented as Mean and Standard Deviation. AIS; Adolescent idiopathic scoliosis. *Significant pairwise comparisons between groups (p < 0.05).

Table 3 Peak humerothoracic elevation levels and scapular position at rest for participants with AIS and healthy controls. AIS Mean (SD) degrees

Healthy controls Mean (SD) degrees

Convex/dominant side* Concave/nondominant side*

132.3 (9.3) 135.9 (11.2)

145.2 (8.8) 143.1 (7.1)

Scapular plane

Convex/dominant side* Concave/nondominant side*

127.1 (8.2) 130.6 (9.5)

141.5 (11.1) 139.5 (7.9)

Frontal plane

Convex/dominant side* Concave/nondominant side*

128.6 (9.8) 131.3 (10.2)

141.8 (10.8) 142 (6.7)

Convex/dominant side at rest Concave/nondominant side at rest

35.6 (8.7) 26.4 (6.4)

30.9 (6.3) 26.9 (4.9)

Upward/downward rotation

Convex/dominant side at rest Concave/nondominant side at rest

4.9 (5.5) 4.7 (7)

6 (5.6) 3.7 (5.5)

Anterior/posterior tilt

Convex/dominant side at rest Concave/nondominant side at rest*

14.1 (6.9) 6.2 (7.5)

8.7 (5.3) 13.8 (5.1)

Peak HT elevation Sagittal plane

Scapular Kinematics Internal/external rotation

Note. AIS, Adolescents Idiopathic Scoliosis; HT, humerothoracic elevation; SD, standard deviation. * Indicates statistically significant pairwise comparisons.

Please cite this article in press as: Turgut, E., et al. Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation. J. Biomech. (2017), http://dx.doi.org/10.1016/j.jbiomech.2017.07.029

E. Turgut et al. / Journal of Biomechanics xxx (2017) xxx–xxx

(Armijo-Olivo et al., 2011). Similar to the majority of findings of previous studies on subjects with shoulder pathologies, the scapula was more downwardly rotated on the concave side. Previous studies using a similar data collection method have reported differences in upward rotation that were less than 5° in a group of patients with shoulder impingement syndrome compared with healthy subjects (Ludewig and Cook, 2000; McClure et al., 2006). However, since there is no clear relationship between altered scapular movement and a specific pathology, the findings should be interpreted with care (McQuade et al., 2016). Our findings showed kinematic alterations occur in asymptomatic group of participants with AIS but the alterations should not be described as abnormal motion or indicating unstable scapula. Rather, it should be suggested as simply kinematic variability for double curve pattern scoliosis. On the other hand, considering the potential progressive nature of the spinal deformity, it is important to evaluate and address possible shoulder dysfunction during rehabilitation of patients with AIS. In this study, participants with AIS revealed decreased scapular upward rotation and accompanying decreased peak humerothoracic elevation on the concave side. For the convex side, decreased scapular posterior tilt were more obvious at higher ranges (>90°) of humerothoracic elevation. For the concave side, the increased scapular posterior tilt was observed at rest and during early stages of elevation. However, decreased scapular posterior tilt was obvious at higher ranges of humerothoracic elevation. Therefore, overhead shoulder activities such as throwing or swimming may theoretically place an increased demand on the shoulder complex of individuals with AIS. The scapular position at rest was also altered in AIS when compared to healthy controls. In asymptomatic subjects, the resting position of the scapula can be influenced by dominancy or participating in overhead sports (Oyama et al., 2008). Research to date has been focused on assessing scapular position and orientation by using visual assessments such as the Walter Reed Visual Assessment Scale for scoliotic patients only in the resting position (Pineda et al., 2006). However, considering scapular alterations found in the AIS, clinicians should also observe scapular movements while asking patients elevate their arm in different movement planes. The alterations in scapular kinematics among the three movement planes of elevation that we assessed were more obvious for frontal plane recordings. This study had some limitations. The findings of this study only apply to adolescents with AIS who have moderate curve magnitude and double curve pattern with no shoulder related symptoms; thus, are not applicable to subjects who have more severe curve and symptoms. Also, for scapular plane elevation, a standardized scapular movement plane was used rather than individually predetermined movement plane while resting scapular orientation was different between study groups. Future research could incorporate scapular muscle activities to enhance the knowledge regarding scapular behavior in AIS and help the understanding of observed alterations in scapular kinematics. In conclusion, scapular movement adaptation was demonstrated in individuals with double curve pattern idiopathic scoliosis. The scapula was more internally rotated and anteriorly tilted on the convex side, and more externally, downwardly rotated, and posteriorly tilted on the concave side in participants with AIS when compared to healthy controls. Additionally, decreased peak humerothoracic elevation and altered scapular posterior tilt on concave side in the resting position were observed in participants with AIS. Therefore, future research is needed to explore the possible effect of scapular movement adaptation on upper extremity function or dysfunction in AIS.

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Acknowledgements This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors. Conflict of interest statement The authors certify that they have no affiliations with or financial involvement in any organization or entity with a direct financial interest in the subject matter or materials discussed in the article. No foundation funds were received in support of this work. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. The study was approved by the University of Hacettepe Research Ethics Board GO 16/80–25 on March 22, 2016. The patients were informed regarding the treatment and its potential benefits as well as evaluation methods; and thereby, signed informed consent forms were obtained. The Manuscript submitted does not contain information about medical device(s)/drug(s). References Adler, N., Bleck, E., Rinsky, L., Young, W., 1986. Balance reactions and eye–hand coordination in idiopathic scoliosis. J. Orthop. Res. 4, 102–107. Armijo-Olivo, S., Warren, S., Fuentes, J., Magee, D.J., 2011. Clinical relevance vs. statistical significance: Using neck outcomes in patients with temporomandibular disorders as an example. Manual Therapy 16, 563–572. Ayhan, C., Turgut, E., Baltaci, G., 2015. Distal radius fractures result in alterations in scapular kinematics: A three-dimensional motion analysis. Clin. Biomech. 30, 296–301. Barrack, R.L., Wyatt, M.P., Whitecloud III, T.S., Burke, S.W., Roberts, J.M., Brinker, M. R., 1988. Vibratory hypersensitivity in idiopathic scoliosis. J. Pediatr. Orthopaed. 8, 389–395. Beaulieu, M., Toulotte, C., Gatto, L., Rivard, C.-H., Teasdale, N., Simoneau, M., Allard, P., 2009. Postural imbalance in non-treated adolescent idiopathic scoliosis at different periods of progression. Eur. Spine J. 18, 38–44. Borstad, J.D., Ludewig, P.M., 2005. The effect of long versus short pectoralis minor resting length on scapular kinematics in healthy individuals. J. Orthop. Sports Phys. Ther. 35, 227–238. Byl, N.N., Gray, J.M., 1993. Complex balance reactions in different sensory conditions: adolescents with and without idiopathic scoliosis. J. Orthop. Res. 11, 215–227. Dayanidhi, S., Orlin, M., Kozin, S., Duff, S., Karduna, A., 2005. Scapular kinematics during humeral elevation in adults and children. Clin. Biomech. 20, 600–606. Goldberg, C.J., Kaliszer, M., Moore, D.P., Fogarty, E.E., Dowling, F.E., 2001. Surface topography, Cobb angles, and cosmetic change in scoliosis. Spine 26, E55–E63. Grubb, S.A., Lipscomb, H.J., 1992. Diagnostic findings in painful adult scoliosis. Spine 17, 518–527. Haik, M.N., Alburquerque-Sendín, F., Camargo, P.R., 2014. Reliability and minimal detectable change of 3-dimensional scapular orientation in individuals with and without shoulder impingement. J. Orthop. Sports Phys. Ther. 44, 341–349. Herman, R., Mixon, J., Fisher, A., Maulucci, R., Stucyk, J., 1985. Idiopathic scoliosis and the central nervous system: A motor control problem: The Harrington lecture, 1983 Scoliosis Research Society. Spine 10, 1–14. Inman, V.T., Saunders, J.B., Abbott, L.C., 1996. Observations of the function of the shoulder joint. 1944. Clin. Orthop. Relat. Res. 330, 3–12. Karduna, A.R., McClure, P.W., Michener, L.A., Sennett, B., 2001. Dynamic measurements of three-dimensional scapular kinematics: A validation study. J. Biomech. Eng. 123, 184–190. Keessen, W., Crowe, A., Hearn, M., 1992. Proprioceptive accuracy in idiopathic scoliosis. Spine 17, 149–155. Kibler, W.B., 1998. The role of the scapula in athletic shoulder function. Am. J. Sports Med. 26, 325–337. Lao, M.L., Chow, D.H., Guo, X., Cheng, J.C., Holmes, A.D., 2008. Impaired dynamic balance control in adolescents with idiopathic scoliosis and abnormal somatosensory evoked potentials. J. Pediatr. Orthopaed. 28, 846–849. LeBlanc, R., Labelle, H., Rivard, C.-H., Poitras, B., 1997. Relation between adolescent idiopathic scoliosis and morphologic somatotypes. Spine 22, 2532–2536. Lin, J.-J., Chen, W.-H., Chen, P.-Q., Tsauo, J.-Y., 2010. Alteration in shoulder kinematics and associated muscle activity in people with idiopathic scoliosis. Spine 35, 1151–1157. Ludewig, P.M., Cook, T.M., 2000. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys. Ther. 80, 276–291.

Please cite this article in press as: Turgut, E., et al. Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation. J. Biomech. (2017), http://dx.doi.org/10.1016/j.jbiomech.2017.07.029

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E. Turgut et al. / Journal of Biomechanics xxx (2017) xxx–xxx

Ludewig, P.M., Reynolds, J.F., 2009. The association of scapular kinematics and glenohumeral joint pathologies. J. Orthopaed. Sports Phys. Therapy 39, 90– 104. Martinez-Liorens, J., Ramirez, M., Colomina, M., Bago, J., Molina, A., Caceres, E., Gea, J., 2010. Muscle dysfunction and exercise limitation in adolescent idiopathic scoliosis. Eur. Respir. J. 36, 393–400. McClure, P.W., Michener, L.A., Karduna, A.R., 2006. Shoulder function and 3dimensional scapular kinematics in people with and without shoulder impingement syndrome. Phys. Ther. 86, 1075–1090. McQuade, K.J., Borstad, J., de Oliveira, A.S., 2016. Critical and theoretical perspective on scapular stabilization: What does it really mean, and are we on the right track? Phys. Ther. 96, 1162–1169. Nault, M.-L., Allard, P., Hinse, S., Le Blanc, R., Caron, O., Labelle, H., Sadeghi, H., 2002. Relations between standing stability and body posture parameters in adolescent idiopathic scoliosis. Spine 27, 1911–1917. Oyama, S., Myers, J.B., Wassinger, C.A., Daniel Ricci, R., Lephart, S.M., 2008. Asymmetric resting scapular posture in healthy overhead athletes. J. Athletic Train. 43, 565–570. Pineda, S., Bago, J., Gilperez, C., Climent, J.M., 2006. Validity of the Walter Reed Visual Assessment Scale to measure subjective perception of spine deformity in patients with idiopathic scoliosis. Scoliosis 1, 1–18.

Sahlstrand, T., Örtengren, R., Nachemson, A., 1978. Postural equilibrium in adolescent idiopathic scoliosis. Acta Orthop. Scand. 49, 354–365. Samuelsson, L., Noren, L., 1997. Trunk rotation in scoliosis the influence of curve type and direction in 150 children. Acta Orthop. Scand. 68, 273–276. Stokes, I.A., 1994. Three-dimensional terminology of spinal deformity: A report presented to the scoliosis research society by the scoliosis research society working group on 3-D terminology of spinal deformity. Spine 19, 236–248. Theodoridis, D., Ruston, S., 2002. The effect of shoulder movements on thoracic spine 3D motion. Clin. Biomech. 17, 418–421. Turgut, E., Pedersen, Ø., Duzgun, I., Baltaci, G., 2016. Three-dimensional scapular kinematics during open and closed kinetic chain movements in asymptomatic and symptomatic subjects. J. Biomech. 49, 2770–2777. Weinstein, S.L., Dolan, L.A., Cheng, J.C.Y., Danielsson, A., Morcuende, J.A., 2008. Adolescent idiopathic scoliosis. Lancet 371, 1527–1537. Wu, G., van der Helm, F.C., Veeger, H.E., Makhsous, M., Van Roy, P., Anglin, C., Nagels, J., Karduna, A.R., McQuade, K., Wang, X., Werner, F.W., Buchholz, B., 2005. ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion–Part II: Shoulder, elbow, wrist and hand. J. Biomech. 38, 981–992. Wyatt, M., Barrack, R., Mubarak, S., Whitecloud, T., Burke, S., 1986. Vibratory response in idiopathic scoliosis. Bone Joint J. 68, 714–718.

Please cite this article in press as: Turgut, E., et al. Scapular kinematics in adolescent idiopathic scoliosis: A three-dimensional motion analysis during multiplanar humeral elevation. J. Biomech. (2017), http://dx.doi.org/10.1016/j.jbiomech.2017.07.029