Skip to main content
NCBI home page
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2023 Feb 1.
Published in final edited form as: J Electromyogr Kinesiol. 2019 Aug 23;62:102350. doi: 10.1016/j.jelekin.2019.08.004

Comparison of Glenohumeral Joint Kinematics Between Manual Wheelchair Tasks and Implications on the Subacromial Space: A Biplane Fluoroscopy Study

Joseph D Mozingo 1,2, Mohsen Akbari-Shandiz 2, Meegan G Van Straaten 2, Naveen S Murthy 3, Beth A Schueler 3, David R Holmes III 4, Cynthia H McCollough 3, Kristin D Zhao 2
PMCID: PMC7036020  NIHMSID: NIHMS1539239  PMID: 31481296

Abstract

Scapula and humerus motion associated with common manual wheelchair tasks is hypothesized to reduce the subacromial space. However, previous work relied on either marker-based motion capture for kinematic measures, which is prone to skin-motion artifact; or ultrasound imaging for arthrokinematic measures, which are 2D and acquired in statically-held positions. The aim of this study was to use a fluoroscopy-based approach to accurately quantify glenohumeral kinematics during manual wheelchair use, and compare tasks for a subset of parameters theorized to be associated with mechanical impingement. Biplane images of the dominant shoulder were acquired during scapular plane elevation, propulsion, sideways lean, and weight-relief raise in ten manual wheelchair users with spinal cord injury. A computed tomography scan of the shoulder was obtained, and modelbased tracking was used to quantify six-degree-of-freedom glenohumeral kinematics. Axial rotation and superior/inferior and anterior/posterior humeral head positions were characterized for full activity cycles and compared between tasks. The change in the subacromial space was also determined for the period of each task defined by maximal change in the aforementioned parameters. Propulsion, sideways lean, and weight-relief raise, but not scapular plane elevation, were marked by mean internal rotation (8.1°, 10.8°, 14.7°, −49.2° respectively). On average, the humeral head was most superiorly positioned during the weight-relief raise (1.6 ± 0.9 mm), but not significantly different from the sideways lean (0.8 ± 1.1 mm) (p = 0.191), and much of the task was characterized by inferior translation. Scaption was the only task without a defined period of superior translation on average. Pairwise comparisons revealed no significant differences between tasks for anterior/posterior position (task means range: 0.1 – 1.7 mm), but each task exhibited defined periods of anterior translation. There was not a consistent trend across tasks between internal rotation, superior translation, and anterior translation with reductions in the subacromial space. Further research is warranted to determine the likelihood of mechanical impingement during these tasks based on the measured task kinematics and reductions in the subacromial space.

Keywords: Shoulder, Wheelchair, Kinematics, Subacromial Space, Fluoroscopy, Model-Based Tracking

1. Introduction

In individuals with spinal cord injury (SCI) who use a manual wheelchair (MWC), upper extremity function is critical for completion of activities of daily living, and thus independence. Tasks such as weight-relief raises, reaching for and lifting objects, and MWC propulsion are repetitive in nature and often require weight-bearing and prolonged shoulder elevation. Unfortunately, up to 73% of MWC users with SCI report shoulder pain related to these demands (Dyson-Hudson and Kirshblum, 2004; McCasland et al., 2006). Shoulder mechanical impingement, caused by a reduction in the subacromial space, is considered one of several factors which may contribute to the development of pain (Mackenzie et al., 2015; Michener et al., 2003). However, emerging evidence in able-bodied populations indicates that the shoulder elevation range associated with impingement may be lower than the range most commonly associated with symptoms (Lawrence et al., 2019), which underscores the complex nature of shoulder pain and pathology.

Fundamentally, the position of the humerus relative to the scapula (glenohumeral) dictates the proximity of the proximal humerus and coracoacromial arch (which form the subacromial space), and consequently the likelihood of mechanical impingement of the rotator cuff. Based on previous work in able-bodied individuals, the generally accepted mechanism thought to lead to a reduction in the subacromial space during arm elevation includes a decrease in scapula upward rotation and posterior tilt, and an increase in scapula and humerus internal rotation (Flatow et al., 1994; Ludewig and Cook, 2000; Mackenzie et al., 2015; Michener et al., 2003; Werner et al., 2006; Yanai et al., 2006). In addition, excessive glenohumeral superior and anterior translations are theorized to reduce the subacromial space (Deutsch et al., 1996; Ludewig and Cook, 2002; Paletta et al., 1997), but fewer studies provide data to directly support or refute this (Lawrence et al., 2014b; Ludewig and Cook, 2002). Scapulothoracic and glenohumeral rotations consistent with these directions have since been identified in individuals with SCI with and without shoulder pain during weight-relief raises, transfers, and propulsion (Finley et al., 2005; Morrow et al., 2011; Nawoczenski et al., 2012; Riek et al., 2008; Zhao et al., 2015). Common to these studies was use of marker-based motion capture systems for kinematic measures. With such approaches, quantification of long axis rotation of the humerus is particularly challenging due to error from skin-motion artifact (Hamming et al., 2012), and joint translations are typically not measured. Without such information, it remains a challenge to determine and prioritize tasks according to which are more or less likely associated with impingement, and to develop evidence-based interventions to reduce injury risk.

The acromiohumeral distance (minimum distance between the acromion and humerus) has also been quantified for estimating the effect of shoulder joint position on the subacromial space during MWC weight-relief raises (Lin et al., 2014; 2015) and propulsion (Belley et al., 2017). Common to these studies was use of ultrasound imaging for arthrokinematic measures. While this technique and parameter are readily accessible, they fail to capture the 3D nature of the subacromial space by isolating the measurement to a single plane dictated by participant and transducer positioning. Additionally, images are acquired in statically-held positions, limiting the functional relevance of these measures and restricting them to a subset of positions that comprise the full task.

Model-based tracking, using computed tomography (CT) and biplane fluoroscopy represents an alternative approach, and has become the gold standard for noninvasive in vivo quantification of bone motion. By enabling direct visualization of bony anatomy, this technique is free of skin-motion artifact error, and shown to provide accurate glenohumeral kinematic measures with mean absolute and root-mean-square errors less than one millimeter and one degree in situ (Bey et al., 2006; Giphart et al., 2012; Massimini et al., 2011; Zhu et al., 2012). Though the total number of experiment conditions is limited by use of ionizing radiation, relative to the other approaches, this method enables highly accurate 3D quantification of both shoulder joint and arthro-kinematics during dynamic and physiologic motion and loading. The utility of this technique for quantification of both glenohumeral rotations and translations has been demonstrated for simple arm elevation tasks (Bey et al., 2008; Giphart et al., 2013; Kijima et al., 2015). However, application of this technique during more functional and complex shoulder movements, including MWC-based tasks, has not been described.

The first goal of this work was to accurately quantify glenohumeral kinematics associated with a spectrum of MWC-based daily tasks, including scapular plane elevation, MWC propulsion, and two types of pressure reliefs, in individuals with SCI who regularly use a MWC. The second goal was to compare tasks for glenohumeral parameters that have been theorized to cause reductions in the subacromial space, which include specific directions of axial rotation and joint translation, and to assess the relationship between these parameters and changes in the size of the subacromial space. Collectively, these efforts lend initial insights into the likelihood of mechanical impingement associated with common MWC tasks. Though scapulothoracic and glenohumeral motion are both necessary to fully resolve the kinematic basis of impingement, glenohumeral motion directly defines the subacromial space, and was therefore the focus of this study. We hypothesized that: (1) Differences in glenohumeral axial rotation, superior/inferior position, and anterior/posterior position would exist between tasks, and (2) Reduction in the subacromial space would take place during the periods of each task defined by the greatest amount of internal rotation, superior translation, and anterior translation.

2. Methods

2.1. Participants

Following approval by the Mayo Clinic Institutional Review Board, 10 participants with SCI who use a MWC as their primary mode of mobility were enrolled. Participants provided written informed consent prior to partaking in the study. An upper extremity physical exam was conducted by a licensed physical therapist to confirm study eligibility. Inclusion and exclusion criteria are listed in Table 1. Following the physical exam, participants completed the Wheelchair User’s Shoulder Pain Index (WUSPI); a validated self-report survey that quantifies shoulder pain associated with 15 MWC-based activities of daily living using a visual analog scale (Curtis et al., 1995a, b). Participants were between 26 and 58 years of age (mean 45.8 ± 12.5 years) and had used a MWC for 1.5 – 35 years (mean 15.9 ± 10.7 years). Injury levels ranged from T3 to T12. The majority of participants (7 of 10) reported some level of shoulder pain. Complete participant characteristics are listed in Table 2.

Table 1:

Recruitment Criteria.

Inclusion Exclusion
(1) 18 – 60 years of age (1) Cervical referred pain
(2) Diagnosis of SCI at T1 or below (2) Shoulder joint instability
(3) ≥ 1 year of MWC use (3) Adhesive capsulitis (loss of > 25% range of motion)
(4) Independent MWC use (4) History of injury and/or surgery of the tested shoulder in which pre-injury status was not attained
(5) Active shoulder range of motion within limits needed for tasks performed during study (5) Contraindications to radiation exposure
(6) Ability to sit and perform MWC transfers unassisted (6) Seated shoulder height that would preclude fluoroscopic visualization of proximal shoulder bony anatomy
(7) Use of a MWC power-assist device
Open in a new tab

Table 2:

Participant Demographics.

Subject Gender SCI level Age [yr.] Time using MWC [yr.] Body Weight [kg] WUSPI* Resting Subacromial Space [mm]
1 Male T12 56 21 97.2 17.05 11.61
2 Male T3 26 5 75.2 10.43 8.63
3 Male T11 57 29 51.3 52.09 7.15
4 Female T10 53 24 75.9 0 8.55
5 Male T11 57 35 92.9 0 10.07
6 Male T6 36 9 93.63 4.48 9.14
7 Male T3 58 16 76 13.58 10.82
8 Male T4 34 1.5 90.9 46.88 8.68
9 Male T10 53 14 68.8 0 11.78
10 Male T7 28 4 83 7.07 7.32
Total [mean(SD)]: 45.8 (12.5) 15.9 (10.7) 80.5 (13.3) 15.2 (18.1) 9.38 (1.56)
Open in a new tab
*

The WUSPI is a validated self-report survey that quantifies shoulder pain associated with 15 MWC-based activities of daily living using a visual analog scale (Curtis et al., 1995 a, b). A WUSPI total score of 0 indicates no pain during, and/or no completion of, each activity within the last 7 days. Higher scores indicate increased pain and decreased function (max total score of 150).

2.2. Participant Imaging

A CT scan of the dominant shoulder (humerus and scapula) was obtained using a clinical scanner (128-slice SOMATOM Definition Edge; Siemens Healthcare) and clinical shoulder musculoskeletal imaging protocol. The participant was supine with their arms at their side. Imaging was performed in two contiguous spiral scans at 140 kV, and data were reconstructed with 0.75 mm slice thickness and 0.35 mm slice increment. A routine dose level was used (250 quality reference mAs) for the scan range that enclosed the scapula and adjacent proximal humerus. For the scan range that enclosed the remainder of the humerus distal to the scapula, a low dose level was used (20 quality reference mAs). Image volumes were scaled to have 0.35 mm cubic voxels, and 3D models of each bone were created via segmentation (AnalyzePro; Mayo Clinic) (Robb et al., 1989).

Dynamic imaging was performed during MWC-based functional tasks using a clinical biplane fluoroscopy system (Artis zee biplane; Siemens Healthcare). This system and technique were previously shown to be capable of providing accurate glenohumeral kinematic measures with root-mean-square errors less than one millimeter and one degree in situ for joint angular velocities as great as 43°/s and 136°/s, respectively (Mozingo et al., 2018). Selected tasks included one trial each of scapular plane elevation (scaption), MWC propulsion, and two pressure relief maneuvers which included a sideways lean and weight-relief raise (Figure 1). A static image pair was also collected with participants seated in a resting neutral position with hands placed in the lap. Participants completed tasks seated in their personal MWC, with the glenohumeral joint of the dominant arm centered in the image volume. During the sideways lean, participants were positioned such that the glenohumeral joint was captured in the image volume at the end range of the task (Figure 1C). The detectors were positioned at a relative angle of 125° in the same vertical plane (Figure 1). Imaging was performed at a detector entrance air kerma of 1820 nGy/frame using a 48 cm field of view (0.308 mm image pixel size). Tube voltage and current were dynamically modulated by automatic exposure rate control. Images were collected at 15 frames/s in each plane with a 33.3 ms temporal offset between planes (the 2 x-ray sources pulse asynchronously with clinical biplane systems) at a pulse width of 3.2 ms. A calibration cube was statically imaged after trials were complete in order to determine the relative position of the x-ray sources and detectors and define the global coordinate system. Total effective dose from the CT scan and fluoroscopy trials was calculated to be 6.8 mSv and 1.0 mSv, respectively; approximately equivalent to the average dose accumulated in 2.5 years from naturally occurring sources to an individual living in the U.S. (Broga, 2009).

Figure 1: Participant Dynamic Imaging.

Figure 1:

Open in a new tab

The glenohumeral joint of the dominant arm was centered in the image volume of a clinical biplane fluoroscopy system (Artis zee biplane; Siemens Healthcare). Participants completed 4 dynamic tasks including scapular plane elevation (A) (guide post not pictured), propulsion (B) (passive wheelchair ergometer pictured), sideways lean (C), and weight-relief raise (D).

Scaption was performed by aligning the arm in a plane approximately 40° anterior to the coronal plane (Figure 1A). Participants started with the arm by their side and elevated from minimum to maximum achievable elevation, with the palm of the hand facing forward, thumb pointed upward, and elbow fully extended. Participants contacted a vertical post with the arm to facilitate maintenance in the scapular plane during imaging. Propulsion was conducted on a passive wheelchair ergometer, allowing the shoulder to remain in the image volume (Figure 1B). The trial consisted of one propulsion cycle beginning from rest, and started/finished with the participant’s hands at the position where they normally begin/end the push cycle. For the sideways lean, participants applied force to the wheel, pushrim, or armrest with their dominant arm and fully extended their elbow in order to lean, offloading the ipsilateral ischium (Figure 1C). The trial started with the participant in an upright posture with both hands on the wheels/pushrims/armrests. The weight-relief raise was conducted from a seated position, starting with the hands on the wheels, push rims, or arm rests (Figure 1D). Participants pushed up from the chair until their elbows were fully extended, and held at the maximum position. The return from maximum to seated position was not imaged.

Tasks were practiced at a steady pace and completed to a verbal cue to yield an approximate trial duration of 3.5 s in order to limit added kinematic error caused by a temporal offset in biplane images (due to alternating pulses of the 2 x-ray sources), which is a function of joint velocity (Mozingo et al., 2018). This also allowed measurement of small changes in bone position from frame-to-frame for the image acquisition rate used. Average glenohumeral angular velocities were 31°/s ± 7.5°/s (mean ± standard deviation (SD)) (scaption), 55°/s ± 5.5°/s (propulsion), 25°/s ± 10.3°/ s (sideways lean), and 27°/s ± 8.6°/s (weight-relief raise).

2.3. Data Processing

Six degree-of-freedom kinematics of the humerus and scapula were determined by registration of the CT bone models to fluoroscopic image pairs using custom model-based tracking software (Figure 2) (described in Akbari-Shandiz et al., 2019). Briefly, the pose of each 3D model was iteratively adjusted such that its 2D digitally reconstructed radiographs (DRRs) were optimally aligned with its fluoroscopic projection in each calibrated image plane based on edge and intensity similarity criteria. Model position was then manually refined using Autoscoper software (Brown University) (Miranda et al., 2011). Model position was determined for consecutive frames of each trial. Scaption data was analyzed from 40° – 80° of glenohumeral elevation, the consistent range spanned by all participants. 3D coordinates of anatomical landmarks were determined directly from the bone models in order to construct coordinate systems. Local coordinate systems to describe joint rotations were based on International Society of Biomechanics recommendations (Figure 3A) (Wu et al., 2005). The origin of the humerus coordinate system was defined as the center of the best fit sphere to the articular region of the humeral head (Lempereur et al., 2010). For descriptions of joint translations only, a glenoid-centered coordinate system was used for the scapula. The origin and axes were set as the centroid and principal axes of the glenoid surface (Graichen et al., 2000), resulting in anteriorly, superiorly, and laterally directed axes (Figure 3B). Positions of the humeral head center were measured relative to the glenoid centroid, and subtracted from the relative position of the humerus and scapula in neutral position (glenohumeral translation defined as the change between two positions). Glenohumeral kinematic parameters were computed using an XZ’Y” Euler sequence (angle of elevation, plane of elevation, and axial rotation) (Phadke et al., 2011) (Figure 3C). For visual comparison of kinematic time series, participant kinematics were interpolated to have an equal number of points for a given activity, averaged, and normalized to percent activity cycle (humeral head center position displayed in increment nearest to 10% of activity cycle). The subacromial space was quantified in the neutral position by measuring the minimum Euclidean distance from the superior facet (supraspinatus tendon insertion site) of the humerus model to the acromion on the scapula model. The change in the subacromial space was determined for each task during the increment defined by the greatest amount of glenohumeral axial rotation and translation in each direction.

Figure 2: Model-Based Tracking.

Figure 2:

Open in a new tab

Custom model-based tracking software (described in Akbari-Shandiz et al., 2019) was used to register 3D models of the humerus (gray) and scapula (not pictured) to corresponding fluoroscopic image pairs (green). The 3D pose and orientation of the bone model was manipulated such that DRRs of the bone model (magenta) optimally aligned with the 2D bone geometry within each fluoroscopic image based on edge and intensity similarity criteria.

Figure 3: Joint Coordinate Systems and Kinematics.

Figure 3:

Open in a new tab

A: Humerus and scapula ISB anatomical coordinate systems (anterior view). X= anterior +/posterior −, Y= superior +/inferior −, Z= lateral +/medial −. The origin of the humerus was defined as the center of the best fit sphere to the articular region of the humeral head (shaded in orange). B: For glenohumeral positions and translations, the scapula was defined in a glenoid-centered coordinate system based on the centroid and principal axes of the glenoid (left image; sagittal view; Z-axis pointing out of the page). Humeral head center position was defined as the position of the origin of the humerus relative to the origin of the scapula, and normalized to the relative position of the humerus and scapula in neutral position. Anterior/posterior was defined along the X-axis (middle image; superior view), and superior/inferior along the Y-axis (right image; posterior view). C: Glenohumeral elevation defined as rotation about the X-axis (left image; posterior view), plane of elevation as rotation about the Z-axis (middle image; superior view), and axial rotation as rotation about the Y-axis (right image; posterior view).

2.4. Statistical Analysis

Descriptive statistics were quantified for each glenohumeral rotation, and for superior/inferior and anterior/posterior humeral head center positions. Prior to repeated measures analysis, data was examined to ensure that it did not violate the test’s assumptions. Descriptive statistics, histograms, and Q-Q plots were examined and demonstrated that the assumption of normality was fulfilled for each task and kinematic parameter. If the assumption of sphericity was violated, as determined by Mauchly’s W test, the degrees of freedom were corrected using Greenhouse-Geisser estimates of sphericity. Mean and maximum glenohumeral internal/external (I-E) rotation, superior/inferior (S-I) position, and anterior/posterior (A-P) position were compared in separate one-way repeated measures ANOVAs, with task (scaption, propulsion, sideways lean, weight-relief raise) as the within-subject factor. Type I error rate was set at 0.05. When a significant effect of task was found, pairwise comparisons were performed with Bonferroni adjustment.

3. Results

Mean and maximum glenohumeral I-E rotation, S-I position, and A-P position were determined for each participant for a given task. Group means, maximums, minimums, and SDs were also determined for each task and are shown in Figure 6 (kinematic parameters fully reported in Tables A1 and A2 (Appendix)). Group mean time series for glenohumeral rotations and humeral head center positions are displayed in Figures 4 and 5 respectively.

Figure 6: Glenohumeral Kinematic Comparisons.

Figure 6:

Open in a new tab

Mean ± SD (blue), maximum ± SD (orange), minimum ± SD (green) glenohumeral axial rotation and position of the humeral head center relative to the glenoid centroid for each task across participants. Standard deviation determined based on individual participant values. Minimum and maximum values correspond to mean of individual participant maximums/ minimums. (Kinematic parameters are fully reported in Tables A1 and A2, Appendix).

Figure 4: Group Mean Glenohumeral Rotations Time Series.

Figure 4:

Open in a new tab

Group mean glenohumeral rotations as a function of percent of activity during scaption (green), propulsion (blue), sideways lean (black), and weight-relief raise (red). Solid lines indicate group mean and shaded regions indicate ± 1 SD.

Figure 5: Group Mean Time Series of Position of Humeral Head Center Relative to Glenoid Centroid.

Figure 5:

Open in a new tab

Group mean humeral head center position as a function of percent of activity during scaption (green), propulsion (blue), sideways lean (black), and weight-relief raise (red). Positions are plotted in increment nearest to 10% of activity cycle for a given activity (square data points). A positive slope for the line connecting two data points indicates superior (left panel) and anterior (right panel) translation. A negative slope indicates inferior (left panel) and posterior (right panel) translation.

Results of statistical tests are provided with the degrees of freedom, corrected degrees of freedom, test statistic (F-ratio), and p-value (adjusted for multiple comparisons). There were significant effects of task on mean glenohumeral I-E rotation [F(3,27) = 91.54, p < 0.0001], S-I position [F(1.48,13.33) = 7.11], p = 0.012], and A-P position [F(1.99, 17.88) = 3.85, p = 0.041]. I-E rotation means for scaption, propulsion, sideways lean, and weight-relief raise were −49.2°, 8.1°, 10.8°, and 14.7° respectively (Figure 6 top panel), with scaption in mean external rotation. Pairwise comparisons demonstrated significant differences in I-E rotation during scaption relative to each other task (scaption vs. propulsion [p < 0.0001], scaption vs. sideways lean [p < 0.0001], scaption vs. weight-relief raise [p < 0.0001]). S-I position means for scaption, propulsion, sideways lean, and weight-relief raise were 0.05 mm, 0.49 mm, 0.75 mm, and 1.60 mm respectively (Figure 6 middle panel), with superior position greatest in the weight-relief raise. Pairwise comparisons demonstrated significant differences between mean S-I position during weight-relief raise compared to scaption [p = 0.007] and propulsion [p = 0.005], but not sideways lean [p = 0.191]. Mean A-P position was most anterior during scaption (1.72 mm), followed by weight-relief raise (1.12 mm), propulsion (0.89 mm), and sideways leans (0.07 mm) (Figure 6 bottom panel). Although significant effects of task were present for mean A-P position, there were no significant differences in pairwise comparisons.

There were significant effects of task on maximum glenohumeral internal rotation [F(3,27) = 100.25, p < 0.0001] and superior position [F(3, 27) = 10.32, p < 0.0001], but not anterior position [F(3,27) = 1.51, p = 0.234]. Pairwise comparisons for maximum internal rotation and superior position resulted in the same task differences observed for mean parameters. Maximum internal rotation during scaption (−43.6°) was less than propulsion (18.4°, p < 0.0001), sideways lean (18.2°, p < 0.0001), and weight-relief raise (22.7°, p < 0.0001) (Figure 6 top panel). Maximum superior position during the weight-relief raise (3.03 mm) was greater than during scaption (0.98 mm, p = 0.002) and propulsion (1.83 mm, p = 0.006), but not sideways lean (1.88 mm, p = 0.123) (Figure 6 middle panel). Maximum anterior positions were 2.91 mm, 2.84 mm, 2.49 mm, and 1.93 mm for the weight-relief raise, scaption, propulsion, and sideways lean respectively (Figure 6 bottom panel).

Mean resting subacromial space was 9.38 ± 1.56 mm and ranged from 7.15 – 11.78 mm (Table 2). The 10% increment of each task defined by the greatest amount of internal rotation was accompanied by reductions in the subacromial space ≥ 1 mm in 0, 1, 0, and 4 participants during scaption, propulsion (4.40 mm), sideways lean, and weight-relief raise (mean = 1.63 mm), respectively (Table 3). The period of the weight-relief raise characterized by the greatest amount of superior translation was defined by reductions in the subacromial space ≥ 1 mm in 6 of 10 participants (mean = 2.64 mm), but in less than 5 participants for each of the other tasks (scaption n = 3, mean = 2.15 mm; propulsion n = 4, mean = 3.38 mm; sideways lean n = 3; mean = 2.92 mm) (Table 3). A reduction in the subacromial space ≥ 1 mm during the period of greatest anterior translation was measured in one participant during a single task (weight-relief raise, 2.18 mm) (Table 3).

Table 3: Reductions in the Subacromial Space During Maximal Glenohumeral Motion.

For each participant, the 10% increment of each task in which the greatest amount of glenohumeral translation and axial rotation occurred was determined (directions considered separately) (data was interpolated to have an equal number of points across participants for a given activity). The change in the subacromial space was measured over these increments, and reductions ≥ 1 mm were tallied. For measures that met this criterion, the average reduction and standard deviation were quantified.

n Scaption avg. reduction (SD) [mm] n Propulsion avg. reduction (SD) [mm] n Sideways Lean avg. reduction (SD) [mm] n Weight-Relief Raise avg. reduction (SD) [mm]
Glenohumeral Translation Superior 3 2.15 (.97) 4 3.38 (1.53) 3 2.92 (2.43) 6 2.64 (1.49)
Inferior 0 N/A 6 3.25 (1.38) 0 N/A 2 2.39 (1.37)
Anterior 0 N/A 0 N/A 0 N/A 1 2.18
Posterior 3 2.15 (.97) 6 3.10 (.61) 3 3.61 (1.86) 6 3.38 (.99)
Glenohumeral Axial Rotation Internal 0 N/A 1 4.40 0 N/A 4 1.63 (.42)
External 2 2.70 (.35) 2 1.91 (.77) 2 2.03 (1.28) 3 2.86 (2.05)
Open in a new tab

4. Discussion

Previous work demonstrates that shoulder kinematics associated with certain MWC-based activities are consistent with those hypothesized to reduce the subacromial space (Finley et al., 2005; Morrow et al., 2011; Nawoczenski et al., 2012; Riek et al., 2008; Zhao et al., 2015). Glenohumeral parameters, and in particular those that are hypothesized to reduce the space, are particularly challenging to measure using marker-based motion capture, as done in past MWC studies. The acromiohumeral distance has also been measured during MWC use via ultrasound imaging (Belley et al., 2017; Lin et al., 2014), but only provides a 2D estimate of the subacromial space in statically-held positions. Thus, a complete and cohesive description of shoulder motion during MWC use does not exist. This work expands on previous efforts by providing highly accurate fluoroscopy-based measures of glenohumeral rotations as well as humeral head center position and glenohumeral translations associated with MWC use, and examines the relation between these parameters and the subacromial space. Quantification of these metrics will further our understanding of potential for impingement during common MWC-based tasks, and provide useful information for physical therapy based interventions.

4.1. Pressure Relief Maneuvers

The weight-relief raise is consistently studied in previous work comparing shoulder kinematics between different MWC-based activities, perhaps due to the presumed harmful nature of the task which requires supporting ones’ body weight through the upper limbs. In the present study, most participants were in glenohumeral internal rotation over the entire activity (Figure 4 bottom panel), with a group mean of 14.7° (Figure 6 top panel). At the moment of peak loading, Riek et al. and Nawoczenski et al. each measured 15° of internal rotation (median and mean, respectively) in individuals with SCI without shoulder pain (Nawoczenski et al., 2012; Riek et al., 2008). At the same loading event and in a similar cohort, Morrow et al. reported mean external rotation of 10° (Morrow et al., 2011). Despite the apparent difference between studies, in each case, the humerus started in a less internally rotated position compared to the position at peak loading, indicating a relative decrease in external rotation. In the present study, most subjects exhibited a similar trend, with the group mean time series demonstrating an increase in internal rotation from the beginning of the weight-relief until approximately 65% into the activity (Figure 4 bottom panel).

Alternative forms of pressure reliefs, such as sideways and forward leans, have been advocated by some (Morrow et al., 2011; Nawoczenski et al., 2012; Riek et al., 2008), and are intended to reduce the load placed on the upper limb (Paralyzed Veterans of America Consortium for Spinal Cord Medicine, 2005). Though not statistically significant, on average, the humerus was less internally rotated (10.8° vs. 14.7°) and superiorly positioned (0.8 mm vs. 1.6 mm) during the sideways lean compared to the weight-relief raise (Figure 6 top and middle panels), which may be beneficial in terms of providing clearance for structures within the subacromial space. However, in many cases (10 of 10 and 6 of 10 participants during the sideways lean and weight-relief raise, respectively), the period of these tasks defined by the greatest amount of internal rotation was not accompanied by reductions in the subacromial space (Table 3).

4.2. Manual Wheelchair Propulsion

On average, individuals with SCI who regularly use a MWC propel for approximately 1 hour over the course of a day (Sonenblum et al., 2012). Thus, even short periods of a single propulsion cycle defined by reductions in the subacromial space may be detrimental. In the present study, mean glenohumeral axial rotation was 8.1° (internally rotated), with a mean range of motion of 19.3° (Figure 6 top panel), and the task period of maximal internal rotation was not accompanied by reductions (≥ 1 mm) in the subacromial space in 9 of 10 participants (Table 3). Reductions during the task periods of maximal change in elevation and plane of elevation may be worth considering in future studies. Similar to the weight-relief raise, in studies that have used marker-based approaches, the magnitude of glenohumeral axial rotation measured during propulsion tends to be variable. For example, in a study of MWC users with shoulder pain, Zhao et al. identified mean external rotation over the full cycle (mean axial rotation of approximately −25°) (Zhao et al., 2015). However, Cloud et al. reported event means that ranged from −7.2° (external rotation) to 1.1° (internal rotation) (Cloud et al., 2017), despite a similar study population and use of the same type of motion capture system. Interestingly, for primary planes of motion (glenohumeral elevation and plane of elevation), time series from each study were similar in pattern and magnitude to those obtained in the present study (Figure 4 top and middle panels). This discrepancy may be in part due to error in axial rotation measures associated with marker-based techniques.

4.3. Scapular Plane Elevation

Compared to the other tasks, scaption was the only characterized by mean external rotation over the full activity (Figure 4 bottom panel), with a group mean range of −55° to −44° (11°) (Figure 6 top panel; Table A1, Appendix). Small differences in external rotation existed between the start and end of the task, with slightly greater external rotation at the end of the task (maximum elevation) in most participants. Zhao et al. observed a similar trend using skin markers, with a reported mean axial rotation of approximately −50° in individuals with SCI (Zhao et al., 2015), although a lower glenohumeral elevation range was examined. In a study that quantified kinematics using bone-fixed markers, glenohumeral axial rotation was not significantly different between able-bodied individuals with and without symptoms of impingement over the glenohumeral elevation range considered in the present study (Lawrence et al., 2014b). Additionally, in the present study, the increment defined by the greatest amount of internal rotation did not coincide with reductions in the subacromial space ≥ 1 mm (Table 3). However, participants were instructed to complete the task with the thumb pointed upward, which likely limited the amount of axial rotation. It is also important to acknowledge that elevation range directly affects the likelihood of impingement during this task (Giphart et al., 2012). The consistent range spanned by all participants was analyzed in this study, with the minimum starting angle likely limited by the wheelchair itself in some participants. Future studies are needed examining scaption over a broader elevation range and for tasks which are functionally similar, but require greater changes in plane of elevation, such as overhead reach.

4.4. Glenohumeral Positions and Translations

In addition to decreased glenohumeral external rotation, excessive superior and anterior translations of the humerus are theorized to contribute to a reduction in the subacromial space (Deutsch et al., 1996; Ludewig and Cook, 2002). During all four activities, on average, the humeral head was positioned 0 – 2 mm superior relative to neutral (Figure 5 left panel; Figure 6 middle panel), and maximum superior position ranged from 1 mm (scaption) to 3 mm (weight-relief raise) (Figure 6 middle panel). Interestingly, scaption was the only task that had no period defined by superior translation on average (Figure 5 left panel). Though no joint translation data is available to compare to for propulsion and pressure relief maneuvers, there are some studies that have used biplane fluoroscopy to measure humeral head center position during arm elevation. In able-bodied participants, Giphart et al. reported an S-I position range of 2.5 mm (−0.8 – 1.7 mm) during scaption (Giphart et al., 2013). The values measured in the present study were comparable, with a mean of 0.05 mm and range of 1.9 mm (−0.9 – 1 mm) (Figure 6 middle panel; Table A2, Appendix). During forward flexion, the authors measured an S-I position range of 3 mm (−0.8 – 2.2mm) (Giphart et al., 2013). In the present study, during propulsion, there was mean S-I position of 0.5 mm and range of 2.8 mm (−1 – 1.8 mm) (Figure 6 middle panel; Table A2, Appendix). Similar to Giphart et al., during tasks in which the glenohumeral plane of elevation undergoes greater change (forward flexion and propulsion), the range of S-I position was increased relative to that measured during scaption, perhaps indicating less joint stability during tasks that require shifting between planes. Superior position measured during weight-relief raises was significantly greater than that measured during scaption and propulsion, with mean and maximum S-I positions of 1.6 mm and 3 mm, respectively (Figure 6 middle panel). Additionally, the period of greatest superior translation across tasks was the first 10% of the weight-relief raise, however later stages of this task exhibited a trend of inferior translation (Figure 5 left panel).

Mean A-P position differed across activities, but there were no significant differences between activities and considerable variation across participants. The period of greatest anterior translation across tasks was during propulsion from 70 – 80% of the activity cycle, and at least 20% of each task was defined by periods of anterior translation (Figure 5 right panel). During all four activities, on average, the humeral head was positioned 0 – 2 mm anterior relative to neutral (Figure 5 right panel; Figure 6 bottom panel). Giphart et al. identified a mean posterior position of the humeral head with respect to the glenoid midline during both scaption and forward flexion. As arm elevation increased, the direction of translation was inconsistent (scaption) or consistently posterior (forward flexion) relative to the position of the humerus at the start of the activity (Giphart et al., 2013). Differences in the present study may in part reflect differences in study populations (able-bodied vs. SCI), the range of glenohumeral elevation examined, and the approach used to quantify positions. Despite these differences, the range of positions was comparable. Giphart et al. reported ranges of 2.4 mm (scaption) and 3.6 mm (forward flexion) (Giphart et al., 2013). In the present study, ranges of 2.1 mm (scaption) and 3.2 mm (propulsion) were obtained (Figure 6 bottom panel; Table A2, Appendix). Though a similar A-P position range was found as in able-bodied participants, the finding of anterior translation and average anterior positioning of the humeral head warrants further research to determine whether this is characteristic of certain MWC-based tasks and/or SCI.

A consistent trend of subacromial space reduction during the periods of each task defined by the greatest amount of glenohumeral superior and anterior translation was not identified in the present study. During the weight-relief raise, in 8 of 10 participants, the period of maximum translation in the S-I direction occurred in conjunction with a mean space reduction of 2.64 mm (6 superior/2 inferior; Table 3). However, during propulsion, the direction of translation associated with reductions was divided and more often in the inferior direction (4 superior/6 inferior; mean reduction > 3 mm; Table 3). Interestingly, during both tasks, appreciable reductions seldom occurred over the period of maximum anterior translation as theorized in the literature, but often did overlap with the period of maximum posterior translation (Table 3). Using ultrasound, Lin et al. identified an average reduction of 1.78 mm in the acromiohumeral distance in a static weight-relief position compared to neutral (Lin et al., 2014), but kinematic changes were not evaluated. Based on the resting subacromial space range of 7 – 12 mm measured in the present study (Table 2), it is possible that the measured reductions would result in mechanical impingement in some participants, given that a subacromial space ≤ 5 mm is historically considered pathological (Weiner and Macnab, 1970). Reductions in the space were less common over the period of maximum translation during scaption and sideways lean, independent of direction.

4.5. Limitations

This study had limitations that should be considered. First, tasks were completed at a controlled rate rather than a self-selected speed. Due to alternating pulsing of each x-ray source (characteristic of clinical biplane fluoroscopy systems), there is a temporal offset between corresponding biplane images (Bushberg et al., 2011). This offset results in added kinematic error during conventional model-based tracking, which assumes synchrony of acquired image pairs. Task speeds were regulated to mitigate this effect and limit added error, and are predicted to add 0.4 – 0.81 mm and 0.15 – 0.26° error in glenohumeral kinematic measures (Mozingo et al., 2018). It is possible that participants moved differently as a result of this constraint. However, participants were given ample time to practice the tasks at a natural speed, and were observed for consistency during the regulated speed prior to imaging. Second, propulsion trials were conducted on a passive wheelchair ergometer rather than over ground. Though friction and inertial properties are not equal between these conditions, use of ergometers is common practice in MWC research, and was necessary to allow propulsion to take place within the image volume. Third, because participants completed one trial per task, in vivo test-retest reliability could not be assessed. However, by limiting each task to a single trial, this allowed comparison of several different tasks of daily living (for a given total radiation exposure), which was prioritized in this study. Last, the findings of this study should be evaluated in light of the sample size, and heterogeneity in SCI injury and shoulder pain levels in this cohort (Table 2), which may have contributed to variation in the reported measures. For example, though there was a significant effect of task on mean A-P humeral position, no pairwise comparisons were significant.

4.6. Conclusions

This study established glenohumeral kinematics during a spectrum of functional MWC tasks using a highly accurate fluoroscopy-based approach. To our knowledge, this is also the first study to quantify and compare humeral head center position and glenohumeral joint translations associated with MWC tasks. The sideways lean, one of the tested pressure relief maneuvers, was not significantly different from the weight-relief raise for glenohumeral parameters, but participants were in less glenohumeral internal rotation and the humeral head center was positioned less superiorly on average. Future studies are needed to investigate the kinematics of the trailing arm during the sideways lean to fully compare these maneuvers. During wheelchair propulsion, the amount of glenohumeral internal rotation of the humerus changed over the course of the activity, with consistent relative glenohumeral internal rotation and anterior translation during later stages of the activity cycle. The humeral head center was positioned significantly less superiorly during scaption and propulsion compared to the weight-relief raise, but scaption was the only task without a defined period of superior translation on average. The results of the present study did not demonstrate a consistent association between internal rotation, superior translation, or anterior translation with reductions in the subacromial space when considering all tasks. Further research is needed to determine the comparative likelihood of mechanical impingement resulting from task-specific kinematic parameters and reductions in the subacromial space over the full activity cycle.

Supplementary Material

1

Acknowledgments

This study was supported by NIH/NIAMS T32 AR56950 and Minnesota Partnership for Biotechnology and Medical Genomics (MNP IF #14.02). We thank Mark Hindal, R.T.(R) for assistance with data collection, and Ryan Lennon, M.S. for statistical support.

Footnotes

Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Conflict of interest statement

All authors declare no conflict of interest.

References

  1. Akbari-Shandiz M, Lawrence RL, Ellingson AM, Johnson CP, Zhao KD, Ludewig PM. MRI vs CT-based 2D-3D auto-registration accuracy for quantifying shoulder motion using biplane video-radiography. J Biomech. 2019;82:375–80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Belley AF, Gagnon DH, Routhier F, Roy JS. Ultrasonographic measures of the acromiohumeral distance and supraspinatus tendon thickness in manual wheelchair users with spinal cord injury. Arch Phys Med Rehabil. 2017;98(3):517–24. [DOI] [PubMed] [Google Scholar]
  3. Bey MJ, Kline SK, Zauel R, Lock TR, Kolowich PA. Measuring Dynamic In-Vivo Glenohumeral Joint Kinematics: Technique And Preliminary Results. J Biomech. 2008;41(3):711–4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bey MJ, Zauel R, Brock SK, Tashman S. Validation of a new model-based tracking technique for measuring three-dimensional, in vivo glenohumeral joint kinematics. J Biomech Eng. 2006;128(4):604–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Broga D Ionizing radiation exposure of the population of the United States. Med Phys. 2009; 36(11):5375. [Google Scholar]
  6. Bushberg JT, Seibert JA, Leidholdt EM, Boone JM. The Essential Physics of Medical Imaging: Wolters Kluwer Health; 2011. [Google Scholar]
  7. Cloud BA, Zhao KD, Ellingson AM, Nassr A, Windebank AJ, An KN. Increased Seat Dump Angle in a Manual Wheelchair Is Associated With Changes in Thoracolumbar Lordosis and Scapular Kinematics During Propulsion. Arch Phys Med Rehabil. 2017;98(10):2021–7 e2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Curtis KA, Roach KE, Applegate EB, Amar T, Benbow CS, Genecco TD, et al. Development of the Wheelchair User’s Shoulder Pain Index (WUSPI). Paraplegia. 1995a;33(5):290–3. [DOI] [PubMed] [Google Scholar]
  9. Curtis KA, Roach KE, Applegate EB, Amar T, Benbow CS, Genecco TD, et al. Reliability and validity of the Wheelchair User’s Shoulder Pain Index (WUSPI). Paraplegia. 1995b;33(10):595–601. [DOI] [PubMed] [Google Scholar]
  10. Deutsch A, Altchek DW, Schwartz E, Otis JC, Warren RF. Radiologic measurement of superior displacement of the humeral head in the impingement syndrome. J Shoulder Elbow Surg. 1996;5(3):186–93. [DOI] [PubMed] [Google Scholar]
  11. Dyson-Hudson TA, Kirshblum SC. Shoulder pain in chronic spinal cord injury, Part I: Epidemiology, etiology, and pathomechanics. J Spinal Cord Med. 2004;27(1):4–17. [DOI] [PubMed] [Google Scholar]
  12. Finley MA, McQuade KJ, Rodgers MM. Scapular kinematics during transfers in manual wheelchair users with and without shoulder impingement. Clinical Biomechanics. 2005;20(1):32–40. [DOI] [PubMed] [Google Scholar]
  13. Flatow EL, Soslowsky LJ, Ticker JB, Pawluk RJ, Hepler M, Ark J, et al. Excursion of the rotator cuff under the acromion. Patterns of subacromial contact. Am J Sports Med. 1994;22(6):779–88. [DOI] [PubMed] [Google Scholar]
  14. Giphart JE, Brunkhorst JP, Horn NH, Shelburne KB, Torry MR, Millett PJ. Effect of plane of arm elevation on glenohumeral kinematics: a normative biplane fluoroscopy study. J Bone Joint Surg Am. 2013;95(3):238–45. [DOI] [PubMed] [Google Scholar]
  15. Giphart JE, van der Meijden OA, Millett PJ. The effects of arm elevation on the 3-dimensional acromiohumeral distance: a biplane fluoroscopy study with normative data. Journal of shoulder and elbow surgery / American Shoulder and Elbow Surgeons [et al. ]. 2012;21(11):1593–600. [DOI] [PubMed] [Google Scholar]
  16. Graichen H, Stammberger T, Bonel H, Haubner M, Englmeier KH, Reiser M, et al. Magnetic resonance-based motion analysis of the shoulder during elevation. Clin Orthop Relat Res. 2000370):154–63. [DOI] [PubMed] [Google Scholar]
  17. Hamming D, Braman JP, Phadke V, LaPrade RF, Ludewig PM. The accuracy of measuring glenohumeral motion with a surface humeral cuff. J Biomech. 2012;45(7):1161–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kijima T, Matsuki K, Ochiai N, Yamaguchi T, Sasaki Y, Hashimoto E, et al. In vivo 3-dimensional analysis of scapular and glenohumeral kinematics: comparison of symptomatic or asymptomatic shoulders with rotator cuff tears and healthy shoulders. J Shoulder Elbow Surg. 2015;24(11):1817–26. [DOI] [PubMed] [Google Scholar]
  19. Lawrence RL, Braman JP, Ludewig PM. The impact of decreased scapulothoracic upward rotation on subacromial proximities. J Orthop Sports Phys Ther. 2019;49(3):180–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lawrence RL, Braman JP, Staker JL, Laprade RF, Ludewig PM. Comparison of 3-dimensional shoulder complex kinematics in individuals with and without shoulder pain, part 2: glenohumeral joint. J Orthop Sports Phys Ther. 2014b;44(9):646–55, B1–3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lempereur M, Leboeuf F, Brochard S, Rousset J, Burdin V, Remy-Neris O. In vivo estimation of the glenohumeral joint centre by functional methods: accuracy and repeatability assessment. J Biomech. 2010;43(2):370–4. [DOI] [PubMed] [Google Scholar]
  22. Lin YS, Boninger ML, Day KA, Koontz AM. Ultrasonographic measurement of the acromiohumeral distance in spinal cord injury: Reliability and effects of shoulder positioning. J Spinal Cord Med. 2015;38(6):700–08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lin YS, Boninger M, Worobey L, Farrokhi S, Koontz A Effects of repetitive shoulder activity on the subacromial space in manual wheelchair users. BioMed Res Int. 2014;2014:1–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ludewig PM, Cook TM. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther. 2000;80(3):276–91. [PubMed] [Google Scholar]
  25. Ludewig PM, Cook TM. Translations of the humerus in persons with shoulder impingement symptoms. J Orthop Sports Phys Ther. 2002;32(6):248–59. [DOI] [PubMed] [Google Scholar]
  26. Mackenzie TA, Herrington L, Horlsey I, Cools A. An evidence-based review of current perceptions with regard to the subacromial space in shoulder impingement syndromes: Is it important and what influences it? Clin Biomech (Bristol, Avon). 2015;30(7):641–8. [DOI] [PubMed] [Google Scholar]
  27. Massimini DF, Warner JJ, Li G. Non-invasive determination of coupled motion of the scapula and humerus--an in-vitro validation. J Biomech. 2011;44(3):408–12. [DOI] [PubMed] [Google Scholar]
  28. McCasland LD, Budiman-Mak E, Weaver FM, Adams E, Miskevics S. Shoulder pain in the traumatically injured spinal cord patient: evaluation of risk factors and function. J Clin Rheumatol. 2006;12(4):179–86. [DOI] [PubMed] [Google Scholar]
  29. Michener LA, McClure PW, Karduna AR. Anatomical and biomechanical mechanisms of subacromial impingement syndrome. Clinical Biomechanics. 2003;18(5):369–79. [DOI] [PubMed] [Google Scholar]
  30. Miranda DL, Schwartz JB, Loomis AC, Brainerd EL, Fleming BC, Crisco JJ. Static and dynamic error of a biplanar videoradiography system using marker-based and markerless tracking techniques. J Biomech Eng. 2011;133(12):121002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Morrow MM, Kaufman KR, An KN. Scapula kinematics and associated impingement risk in manual wheelchair users during propulsion and a weight relief lift. Clin Biomech (Bristol, Avon). 2011;26(4):352–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mozingo JD, Akbari Shandiz M, Marquez FM, Schueler BA, Holmes DR 3rd, McCollough CH, et al. Validation of imaging-based quantification of glenohumeral joint kinematics using an unmodified clinical biplane fluoroscopy system. J Biomech. 2018;71(306–12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nawoczenski DA, Riek LM, Greco L, Staiti K, Ludewig PM. Effect of shoulder pain on shoulder kinematics during weight-bearing tasks in persons with spinal cord injury. Arch Phys Med Rehabil. 2012;93(8):1421–30. [DOI] [PubMed] [Google Scholar]
  34. Paletta GA Jr., Warner JJ, Warren RF, Deutsch A, Altchek DW. Shoulder kinematics with two-plane x-ray evaluation in patients with anterior instability or rotator cuff tearing. J Shoulder Elbow Surg. 1997;6(6):516–27. [DOI] [PubMed] [Google Scholar]
  35. Paralyzed Veterans of America Consortium for Spinal Cord Medicine. Preservation of Upper Limb Function Following Spinal Cord Injury: A Clinical Practice Guideline for Health-Care Professionals. The Journal of Spinal Cord Medicine. 2005;28(5):434–70. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Phadke V, Braman JP, LaPrade RF, Ludewig PM. Comparison of glenohumeral motion using different rotation sequences. J Biomech. 2011;44(4):700–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Riek LM, Ludewig PM, Nawoczenski DA. Comparative shoulder kinematics during free standing, standing depression lifts and daily functional activities in persons with paraplegia: considerations for shoulder health. Spinal Cord. 2008;46(5):335–43. [DOI] [PubMed] [Google Scholar]
  38. Robb RA, Hanson D, Karwoski R, Larson A, Workman E, Stacy M. Analyze: a comprehensive, operator-interactive software package for multidimensional medical image display and analysis. Comput Med Imaging Graph. 1989;13(6):433–54. [DOI] [PubMed] [Google Scholar]
  39. Sonenblum SE, Sprigle S, Lopez RA. Manual Wheelchair Use: Bouts of Mobility in Everyday Life. Rehabilitation Research and Practice. 2012;2012(753165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Weiner DS, Macnab I Superior migration of the humeral head: a radiological aid in the diagnosis of tears of the rotator cuff. J Bone Joint Surg Br. 1970;52(3):524–27. [PubMed] [Google Scholar]
  41. Werner CML, Blumenthal S, Curt A, Gerber C. Subacromial pressures in vivo and effects of selective experimental suprascapular nerve block. J Shoulder Elbow Surg. 2006;15(3):319–23. [DOI] [PubMed] [Google Scholar]
  42. Wu G, van der Helm FC, Veeger HE, Makhsous M, Van Roy P, Anglin C, et al. 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. 2005;38(5):981–92. [DOI] [PubMed] [Google Scholar]
  43. Yanai T, Fuss FK, Fukunaga T. In vivo measurements of subacromial impingement: substantial compression develops in abduction with large internal rotation. Clin Biomech (Bristol, Avon). 2006;21(7):692–700. [DOI] [PubMed] [Google Scholar]
  44. Zhao KD, Van Straaten MG, Cloud BA, Morrow MM, An K-N, Ludewig PM. Scapulothoracic and Glenohumeral Kinematics During Daily Tasks in Users of Manual Wheelchairs. Frontiers in Bioengineering and Biotechnology. 2015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zhu Z, Massimini DF, Wang G, Warner JJ, Li G. The accuracy and repeatability of an automatic 2D-3D fluoroscopic image-model registration technique for determining shoulder joint kinematics. Med Eng Phys. 2012;34(9):1303–9. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

1
NIHMS1539239-supplement-1.docx (7.7MB, docx)

RESOURCES