- Email: [email protected]
Shoulder Ultrasound Abnormalities, Physical Examination Findings, and Pain in Manual Wheelchair Users With Spinal Cord Injury
2086
ORIGINAL ARTICLE
Shoulder Ultrasound Abnormalities, Physical Examination Findings, and Pain in Manual Wheelchair Users With Spinal Cord Injury Steven W. Brose, DO, Michael L. Boninger, MD, Bradley Fullerton, MD, Thane McCann, MD, Jennifer L. Collinger, BSE, Bradley G. Impink, BSE, Trevor A. Dyson-Hudson, MD ABSTRACT. Brose SW, Boninger ML, Fullerton B, McCann T, Collinger JL, Impink BG, Dyson-Hudson TA. Shoulder ultrasound abnormalities, physical examination findings, and pain in manual wheelchair users with spinal cord injury. Arch Phys Med Rehabil 2008;89:2086-93. Objectives: To investigate the presence of ultrasound (US) abnormalities in manual wheelchair users with spinal cord injury (SCI) using a quantitative Ultrasound Shoulder Pathology Rating Scale (USPRS). To investigate physical examination (PE) findings using a quantitative Physical Examination of the Shoulder Scale (PESS), and to obtain data about pain and other subject characteristics such as age, years with SCI, and weight. Design: Case series. Setting: National Veterans’ Wheelchair Games 2005 and 2006. Participants: Volunteer sample of manual wheelchair users with SCI participating in the National Veterans’ Wheelchair Games. Interventions: Not applicable. Main Outcome Measures: Presence of relationships between US findings, PE findings, pain, and subject characteristics. Results: The USPRS correlated with age, duration of SCI, and weight (all P⬍.01), and showed a positive trend with the total Wheelchair User’s Shoulder Pain Index (WUSPI) score (r⫽.258, P⫽.073). Several US findings related to presence of PE findings for specific structures. The PESS score correlated with the WUSPI (r⫽.679, P⬍.001) and duration of SCI (P⬍.05). The presence of untreated shoulder pain that curtailed activity was noted in 24.5% of subjects, and this was related to increased WUSPI scores (P⫽.002).
From the Department of Physical Medicine and Rehabilitation, University of Pittsburgh Medical Center, Pittsburgh, PA (Brose, Boninger, Collinger); Human Engineering Research Laboratories, Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, PA (Boninger, Collinger, Impink); The Patient-Physician Partnership, Austin, TX (Fullerton); Children’s Hospital of Austin, Austin, TX (Fullerton); Department of Orthopaedics and Rehabilitation, Walter Reed Army Medical Center, Washington, DC (McCann); Thomas Jefferson University, Philadelphia, PA (McCann); Spinal Cord Injury Research, Kessler Medical Rehabilitation Research and Education Center, West Orange, NJ (Dyson-Hudson); Department of Physical Medicine and Rehabilitation, University of Medicine and Dentistry of New Jersey, New Jersey Medical School, Newark, NJ (Dyson-Hudson). Supported by the Veterans Affairs Center of Excellence for Wheelchairs and Associated Rehabilitation (grant no. B3142C), the National Science Foundation (grant no. DGE0333420), the National Institute on Disability and Rehabilitation (grant no. H133N000019), and the Paralyzed Veterans of America. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Reprint requests to Steven W. Brose, DO, Dept of Physical Medicine and Rehabilitation, University of Pittsburgh Medical Center, 3471 Fifth Ave, Ste 201, Pittsburgh PA 15213, e-mail: [email protected]. 0003-9993/08/8911-00154$34.00/0 doi:10.1016/j.apmr.2008.05.015
Arch Phys Med Rehabil Vol 89, November 2008
Conclusions: PE and US abnormalities are common in manual wheelchair users with SCI. The USPRS and PESS demonstrated evidence for external validity and hold promise as research tools. Untreated shoulder pain is common in manual wheelchair users with SCI, and further investigation of this pain is indicated. Key Words: Rehabilitation; Shoulder; Spinal cord injuries; Ultrasonography; Wheelchairs. © 2008 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation ANUAL WHEELCHAIR USERS have increased demands placed on the structures of the shoulder. In addiM tion to neuropathic phenomena, many factors contribute to mechanical shoulder stress. Activities such as transferring the wheelchair in and out of vehicles, bathing, and even dressing contribute to stress on the shoulders. The mechanical forces created by increased intra-articular pressure and repetitive motions necessitated by manual wheelchair mobility are believed to contribute to the development of shoulder pain, impingement syndromes, and rotator cuff injuries.1,2 Weakness in specific muscles can cause an imbalance in the forces placed on the rotator cuff as well as lead to shortening of antagonists to weak muscles.3,4 Another proposed source of increased demand on the shoulders is overuse of structures that compensate for weakness in other muscle groups.4 Persons with tetraplegia use alternative muscle groups for the lost contribution of the normative primary movers for a given task; an example of this phenomenon would be a person with C6 tetraplegia performing inferior reach. This leads to compensatory use of rotator cuff muscles to perform the task previously accomplished by prime movers.5 Established risk factors for shoulder pain in persons with SCI include increased body mass index, duration of injury, and age.6 Investigations have been conducted to identify ways of reducing shoulder related complaints in the wheelchair-using population. Examples of this include identifying which wheelchair propulsion techniques may contribute to progression of shoulder pathology7 and improving wheelchair design. Despite
List of Abbreviations AC MRI PE PESS SCI US USPRS WUSPI
acromioclavicular magnetic resonance imaging physical examination physical examination of the shoulder scale spinal cord injury ultrasound ultrasound shoulder pathology rating scale Wheelchair User’s Shoulder Pain Index
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
the increasing amount of literature in the field, shoulder pain remains common among persons with SCI who use manual wheelchairs, with reported occurrence ranging from 51% to 78%.1,2,4,8-12 Bayley et al1 found a 30% incidence of chronic, persistent shoulder pain during transfers in a cohort of 94 patients with paraplegia. The most common diagnosis in this group was impingement syndrome with subacromial bursitis. Shoulder pathology in persons with SCI is common. Bayley1 found that 65% of subjects with paraplegia who had signs and symptoms of impingement had tears of the rotator cuff. Escobedo et al13 found that 57% of persons with paraplegia had rotator cuff tears and found a significantly higher rate of rotator cuff tear in persons with paraplegia than in uninjured people. A wide variety of other shoulder pathologies have been described by Boninger et al14 in individuals with paraplegia including acromioclavicular joint abnormalities, coracoacromial ligament thickening and edema, subacromial spurs, and distal clavicle osteolysis. Kivimäki and Ahoniemi15 used diagnostic US to demonstrate that the shoulders of persons with SCI have an increased frequency of irregularity and effusion in the glenohumeral joint space compared with individuals without SCI. Given the frequent occurrence of shoulder pain and pathology in persons with SCI, it is important for both clinical and research purposes to have versatile and inexpensive diagnostic technologies available to evaluate shoulder pathology. The accuracy of office-based ultrasonography has been demonstrated compared with MRI for diagnosing shoulder pathology.3,16-24 Iannotti et al19 found that US correctly diagnosed 88% of full thickness rotator cuff tears compared with 95% accuracy of diagnosis with MRI. Partial thickness tears had been diagnosed with 70% accuracy using US compared with 73% using MRI. US was more accurate than MRI in identifying uninjured shoulders, with an accuracy of 80% for US versus 75% for MRI. The utility of individual US signs and maneuvers for evaluating pathology has been examined in individuals without SCI. Jacobson et al20 documented that tendon nonvisualization was 24% sensitive and 100% specific for supraspinatus tear compared with arthroscopy. To obtain the most accurate assessment of pathology, evaluating a combination of US abnormalities has been recommended as opposed to relying on a single sentinel sign.16,20 By combining the signs of cortical surface irregularity and joint fluid presence, Jacobson20 obtained a sensitivity of 60% and specificity of 100% for the diagnosis of supraspinatus tendon tear. US has the advantages of being easy to perform in an office setting, having a low cost of examination, and allowing dynamic examination of joints during motion. The argument of a steep learning curve is sometimes made against the use of US, but there is evidence indicating that a relatively inexperienced ultrasonographer can still obtain accurate results in US of the shoulder.25 The purpose of this study was to investigate the association between shoulder US abnormalities, shoulder pain, subject characteristics, and physical examination findings in a cohort of manual wheelchair– using persons with SCI. We hypothesized that there would be relationships between increasing US scores for pathology, positive physical examination findings, shoulder pain intensity, and subject characteristics associated with rotator cuff pathology such as increasing age, weight, and duration of SCI. To date, no quantitative scale has been developed to evaluate and quantify shoulder pathology using US. To evaluate our hypothesis, a USPRS was developed for this study as a method of quantifying the results of a series of established clinical tests designed to identify shoulder pathology. The scale was developed using known US findings for normative shoulders and common signs of pathology.16,17,19,20,22-27 Further-
2087
more, because no scale for quantifying physical examination abnormalities has been developed to date, we created a physical examination of the shoulder scale to quantify common clinical tests to evaluate shoulder pain. There is no previously developed criterion standard that can be used to evaluate these scales. This article describes the USPRS and PESS and relationships between US findings, physical examination findings, pain, and self-reported subject characteristics. METHODS Subjects A convenience sample of manual wheelchair users with SCI participating in the National Veterans’ Wheelchair Games in 2005 and 2006 was recruited. Subjects were included in the study if they had injury to the spinal cord, used a manual wheelchair as their primary means of mobility, and were between 18 and 65 years of age. Subjects were excluded from study participation if they had a history of traumatic injury to both their upper extremities that limited mobility, or an upperextremity injury that they had otherwise not recovered from. All subjects provided written informed consent before being included in the study in accordance with procedures approved by the institutional review board. Questionnaires Shoulder pain was measured using the WUSPI.28,29 The WUSPI is a 15-item, self-report instrument that provides a personal estimate of shoulder pain experienced during transfers, wheelchair mobility, self-care, and other general activities. Each item is scored using a continuous 10-cm visual analog scale that is anchored at the ends with 0 (no pain) and 10 (worst pain ever experienced). Individual item scores are summed to arrive at a total index score, which ranges from 0 to 150. Each subject also filled out a questionnaire including information about their specific injury, general characteristics such as age and weight, and specific questions regarding the nature of their shoulder pain. All information including level and completeness of SCI was self-reported by using this questionnaire. Physical Examination The PESS score was obtained by performing a series of 11 commonly used physical examination maneuvers for shoulder pathology. The PESS consisted of the following maneuvers: (1) palpation over the bicipital groove/biceps tendon, (2) palpation over the greater tuberosity/supraspinatus tendon, (3) palpation over the acromioclavicular joint, (4) Neer sign, (5) Hawkins-Kennedy impingement sign, (6) painful arc, (7) supraspinatus (Jobe’s or “empty can”) test, (8) resisted external rotation, (9) resisted internal rotation; and the active compression (O’Brien) test for the (10) labrum and (11) AC joint. The Neer, O’Brien, and Hawkins-Kennedy tests were performed as described in the original publications.30-32 The O’Brien tests for the labrum and AC joint were treated as separate tests, because it was noted that some individuals had positive findings on both tests, and hence the 2 parts of this test were scored as separate tests within the PESS. The individual scores of PE tests (appendix 1) were added together to form the PESS for a shoulder. The maximum possible score for a shoulder was 22, and the minimum was 0. The tests were chosen because of their common clinical usage and also because their validity has been investigated previously.33,34 The PESS was performed on both shoulders of each subject by one of several trained physician examiners. The examiners Arch Phys Med Rehabil Vol 89, November 2008
2088
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
finding or characteristic was related to the score in a variable such as the PESS or USPRS, dichotomizations were performed. Some examples of dichotomizations included the presence or absence of untreated shoulder pain, the presence of positive findings in specific clinical tests making up the PESS, the presence of tetraplegia, and the occurrence of complete injury. Differences between dichotomized groups were investigated using a Mann-Whitney U test for nonparametric variable comparison, and a t test for independent samples was used for normally distributed variable analysis. RESULTS
Fig 1. Marked cortical irregularity. Grade 3 on USPRS.
were blind to the results of the questionnaire and WUSPI. All physical examinations were performed with the test subject seated in a wheelchair. US Examination Each participant had US evaluation of a single shoulder. The nondominant side was tested provided there was no prior traumatic injury to the extremity. A single experienced examiner performed all US examinations. The examiner was blind to the results of the questionnaire, WUSPI, and physical examination. A Diasus US Machinea with a transducer 8 to 16MHz was used to collect images. All US examinations were performed with the test subject seated in a wheelchair. The USPRS is a scale based on 5 US signs; 3 signs are static and 2 are dynamic. The static tests were greater tuberosity cortical surface irregularity, supraspinatus tendinopathy, and bicipital tendinopathy. The dynamic tests were supraspinatus impingement and subscapularis/biceps/coracoid impingement. Commonly used signs of pathology on US16,17,19,20,22-27 determined type and degree of pathology. Examples of signs of pathology may include loss of fibrillar pattern for tendinopathy, regions of lucency for a tear, and uneven motion for impingement. A simple ordinal rating scale similar to that used for muscle strength testing was applied to each US sign based on the amount of pathology present. All the scores were summed to form the USPRS for a given shoulder (appendix 2). Figures 1 and 2 provide examples of how to score the USPRS for 2 pathologies. Data Analysis All data analysis was performed using SPSS.b Descriptive analysis was conducted on all variables analyzed for statistical relationships. All correlations were investigated by obtaining the nonparametric Spearman . Correlations between the WUSPI, USPRS, PESS, age, weight, and years with SCI were investigated. To analyze whether the presence or absence of a Arch Phys Med Rehabil Vol 89, November 2008
Subject Characteristics Forty-nine subjects with chronic SCI who used manual wheelchairs as their primary means of mobility participated in the study. The mean subject age ⫾ SD was 44.8⫾9.2 years, and 48 of the 49 individuals who participated in the study were men, which was representative of the participants in the National Veterans’ Wheelchair Games. The average duration with SCI was 16.35⫾9.3 years, and the median was 15.9 years. Average weight was 187.69⫾46.4lb, and the median was 185lb. Complete injuries were reported by 46.9% of subjects (n⫽23), 46.9% had an incomplete injury (n⫽23), and 6.1% were unspecified (n⫽3). Persons with tetraplegia made up 28.6% of the study population (n⫽14), 67.3% had paraplegia (n⫽33), and 4.1% were unspecified (n⫽2). Sixty-seven percent of subjects reported shoulder pain in the last month. Nearly one quarter of the subjects (24.5%) had untreated shoulder pain that curtailed their activity. The only normally distributed variables in this study were height, weight, age, and years with SCI. The USPRS had a Kolmogorov-Smirnov value that indicated it may be normally distributed (.354), but because it is a continuous variable, it was analyzed using nonparametric testing. WUSPI Scores Table 1 displays correlations between the WUSPI, PESS, USPRS, and other variables. Eighty-four percent of subjects
Fig 2. Partial-thickness tear of the supraspinatus tendon. Grade 4 on USPRS.
2089
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose Table 1: Correlations and Statistical Relationships
Scales
USPRS PESS-both shoulders combined WUSPI
Age
Weight
Years With SCI
rs⫽417 P⫽.003* rs⫽.265 P⫽.072 rs⫽.242 P⫽.095
rs⫽.468 P⫽.001* rs⫽.151 P⫽.311 rs⫽.328 P⫽.021*
rs⫽.368 P⫽.009* rs⫽.328 P⫽.024* rs⫽.304 P⫽.034*
Presence of Untreated Shoulder Pain Curtailing Activity
P⫽.811 P⫽.008* P⫽.003*
WUSPI
rs⫽.258 P⫽.073 rs⫽.697 P⬍.001* NA
PESS-US Examined Shoulder
Presence of Complete Injury
Tetraplegia Versus Paraplegia
rs⫽.247 P⫽.095 NA
P⫽.289
P⫽.215
P⫽.592
P⫽.399
NA
P⫽.866
P⫽.575
Abbreviations: NA, not applicable; rs, Spearman’s rho. *P⬍.05.
reported pain on at least 1 item of the WUSPI, which included any score greater than 0 on any item. The mean WUSPI score was 23.0⫾28.5 out of a possible 150, and the median was 8.4. Recorded subject WUSPI scores ranged from 0 to 109. Individuals reporting elbow or shoulder noise during activity had higher WUSPI scores than those without noise in these joints (P⫽.01). The average WUSPI score among individuals reporting shoulder or elbow noise during activity was 33.7, compared with an average WUSPI score of 16 in individuals not reporting noise. Subjects with untreated shoulder pain curtailing activity were also noted to have higher WUSPI scores. The mean WUSPI score of individuals with untreated shoulder pain curtailing their activity was 40.7, compared with a mean score of 16.2 in individuals who did not report untreated pain curtailing activity. The WUSPI correlated with weight and duration of SCI. No relationship was found between the WUSPI and age, whether the subjects had a complete injury, or the presence of tetraplegia versus paraplegia. Physical Examination The mean PESS score, which was the sum of the 11 physical examination scores for both shoulders combined, was 8.98⫾9.69 out of a possible 44 points, and the median was 5. Recorded scores ranged from 0 to 36 points. Figure 3 details the frequencies of positive findings for the 11 physical examination tests making up the PESS. Individuals with shoulder pain in the last month had higher PESS scores than those without pain. The mean PESS score in subjects reporting pain in the last month was 11.1, compared with a PESS score of 4.4 in individuals without shoulder pain in the last month. Individuals with untreated shoulder pain that curtailed their activity also had higher PESS scores (P⫽.008). The mean PESS score in individuals with untreated shoulder pain curtailing activity was 14.6, compared with a PESS score of 6.8 for individuals who did not have untreated shoulder pain curtailing activity. The PESS correlated with the WUSPI and duration of SCI. There was no correlation between the PESS and age or weight. The average sum of the 11 physical examination scores of the right shoulders was 1.99 points higher than that of the left shoulders. The sum of the 11 physical examination scores of each shoulder correlated with the sum of the 11 physical examination scores of the opposing shoulder (r⫽.498; P⫽.001). US Findings All shoulders examined exhibited abnormalities on US. Figure 4 details the frequencies of the 5 abnormalities making up the USPRS. All 5 measures evaluated on the US examina-
tion positively correlated with each other (P⬍.05). The mean total USPRS score was 6.84⫾3.19 out of a possible 20 with a median of 7. USPRS total scores ranged from 2 to 15 points. The USPRS correlated with age, duration of SCI, and weight, and showed a trend in correlation with the WUSPI that did not reach statistical significance. The USPRS was not significantly correlated with the PESS. Although the USPRS did not correlate with the PESS, increasing pathology of several measures of the USPRS was found to relate to the presence of individual signs in PE. One notable finding was that individuals with tenderness at the supraspinatus/greater tuberosity had higher scores for dynamic supraspinatus impingement than those who did not have tenderness (P⫽.039). Individuals with tenderness at this location also had increased greater tuberosity cortical surface irregularity than those who were not tender (P⫽.03). Increased cortical surface irregularity was noted in individuals with a positive Neer sign (P⫽.027). In the same fashion, the presence of a positive Neer sign was associated with higher degrees of supraspinatus tendinopathy on US (P⫽.019). Subjects with a positive resisted external rotation test had higher scores for dynamic supraspinatus impingement (P⫽.016). There was no identifiable relationship between bicipital tendinopathy and tenderness at the bicipital groove.
Fig 3. Physical examination findings.
Arch Phys Med Rehabil Vol 89, November 2008
2090
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
Fig 4. Ultrasound findings.
DISCUSSION The findings of this study confirmed our hypothesis that increasing shoulder pathology visualized on US would be associated with subject characteristics known to be risk factors for shoulder pathology. Increasing age is a known risk factor for shoulder pathology in the non-SCI population.35 The USPRS has evidence for external validity because of its correlation with age, weight, and duration of SCI. Shoulder pathologies have been described to coexist frequently with one another.34,36 The positive intratest correlation of individual tests making up the USPRS provides some evidence of internal consistency in the USPRS. The association of specific findings on the USPRS with certain clinical tests provides evidence that the examinations chosen to form the USPRS were valid choices. The relationship between cortical irregularity and supraspinatus tenderness is a finding worthy of note, because the cortical irregularity sign on US has previously been described as useful in evaluating supraspinatus tear.20 The prevalence of cortical irregularity of the greater tuberosity on US, supraspinatus impingement on US, and positive supraspinatus physical examination tests in this study indicate that pathology in the supraspinatus may be a frequent problem in individuals with SCI. The lack of an association between bicipital tenderness and bicipital tendinopathy appears to concur with literature noting the low sensitivity and specificity of tenderness at the bicipital groove for bicipital pathology.37 The correlation between the total summed PESS for both shoulders and the WUSPI indicates that the PESS has evidence for external validity and may have use for quantifying painful shoulder pathology. Statistical analysis indicates that a portion of the pain measured by the WUSPI may be related to pathology in the structures tested in this PE sequence. The correlation of each shoulder’s PESS with the opposing shoulder indicates that persons with SCI presenting with unilateral shoulder pathology may in fact have underlying bilateral shoulder pathology. This is a topic that warrants further investigation. The relationship of the PESS to pain in the last month and the correlation with the subject’s duration of SCI is further evidence for external validity of the PESS. Arch Phys Med Rehabil Vol 89, November 2008
Our application of the O’Brien PE maneuver involved scoring each portion of the test as a separate item in the PESS, because some subjects had positive findings for both the acromioclavicular and labral portions of the test. The test is sometimes used clinically to differentiate pathologies between these 2 shoulder structures, as opposed to being treated as 2 separate tests. It is reasonable to treat the O’Brien maneuver for the AC joint and labrum as 2 separately scored items in the PESS because shoulder pathologies frequently coexist with one another.34,36 It is possible to use the O’Brien test to evaluate coexisting AC joint and labral pathology. The relationship between the WUSPI and the presence of shoulder pain that has not been treated by a physician and that is curtailing activity is a noteworthy finding of the study. There is a population of persons with SCI who have untreated shoulder pain. Persons with SCI learn to cope with impairments, and it is possible that clinically significant shoulder pain is underappreciated in this group. Roughly one fourth of our subjects had shoulder pain that limited their activity and was not treated by a physician. This lends credence to the assertion that this untreated shoulder pain is clinically significant and has an impact on quality of life. Further investigation of this phenomenon and the ways that it affects individuals with SCI is warranted. Contrary to our hypothesis, a statistically significant correlation between the USPRS and the WUSPI was not supported by the data, although a trend was identified. A lack of statistically significant correlation of the USPRS with pain is not necessarily unexpected. It has been reported that individuals with pathology affecting multiple tendons or with full-thickness tears may have mild to no pain.36 This is seen with increasing frequency as individuals grow older and has been studied with regard to abnormalities in the supraspinatus tendon,38 and 100% of our subject population had pathology of the supraspinatus tendon. Age was not significantly correlated with the WUSPI. Our findings support the assertion that absence of pain does not represent absence of shoulder pathology, and pain may be a marker for future shoulder pathology even if current pathology is not present; this is a topic for further investigation. Furthermore, although the sensation of pain in impingement syndrome is sometimes assumed to be directly related to pathology of the rotator cuff, there is a complex anatomical proximity of several structures that might be sources of pain. Soifer et al39 found that there was a larger concentration of free nerve fibers in the subacromial bursa than the rotator cuff tendon or biceps tendon. It is believed that the presence of inflammatory cytokines or sensitization of the nerve endings in the bursa may sometimes be responsible for the pain associated with impingement syndrome.40-43 Another factor that may contribute to a lack of statistical relationship between the USPRS and the WUSPI is the broad range of activities in the WUSPI that may involve shoulder structures not visualized with US or not examined in this protocol. It is difficult to visualize the posterior aspects of the supraspinatus and infraspinatus, as well as the glenoid labrum. A lack of correlation between the total scores of the USPRS and the PESS is not surprising because a number of tests in the physical examination evaluate structures not represented in the USPRS. Study Limitations Limitations of the study include the selection of a subject population predominantly composed of men participating in athletic events. Further study is needed to determine whether the findings of this study may be generalized to populations broader than this. Although the sample size of 49 subjects was large enough to obtain useful information, a larger sample may
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
(1)
Biceps tendon/bicipital groove tenderness. Palpation of the biceps tendon and bicipital groove is best achieved with the arm in 10° of internal rotation. (2) Supraspinatus tendon/greater tuberosity tenderness. Palpation of the greater tuberosity and supraspinatus insertion is best achieved by slightly extending and internally rotating the arm. The greater tuberosity can be found distal to the anterolateral border of the acromion. (3) Acromioclavicular joint tenderness. Pain with palpation of the acromioclavicular joint. (4) Resisted external, and (5) internal rotation. The subject isometrically attempts rotation against resistance while keeping the palm facing medially and elbow flexed at 90°. (6) Supraspinatus test. Resistance is applied with the patient’s arm abducted to 90°, forward-flexed to 30°, and pronated. The test is positive if pain or weakness is present during resistance. (7) Painful Arc Test. Pain between 60° and 120° of active shoulder abduction in the coronal plane. (8) Neer impingement sign. With the examiner’s opposite hand on the trapezius, the patient’s arm is forcibly elevated through forward flexion by the examiner, causing a jamming of the greater tuberosity against the anterioinferior border of the acromion. The test is positive if it produces pain. (9) Hawkins-Kennedy impingement sign. Slightly flexed at the elbow, the patient’s arm is first elevated forward to 90° and then forcibly medially rotated. This pushes the supraspinatus tendon against the anterior surface of the coracoacromial ligament. The test is positive if the maneuver produces pain. (10) O’Brien Active Compression Test for Acromioclavicular Joint Pathology and (11) Labral Pathology. While seated, the patient is asked to forward-flex the affected arm to 90° with the elbow in full extension. The patient then adducts the arm 10° to 15° medial to the sagittal plane of the body and fully pronates the arm so the thumb points downward; the examiner, standing behind the patient, then applies a downward force to the arm; the maneuver is repeated with the palm fully supinated. The test is positive if pain is elicited during the first maneuver and reduced or eliminated during the second maneuver. The test for acromioclavicular joint is positive if the test elicits pain localized to that location, and the test is positive for the labrum if there is pain or painful clicking described deep within the shoulder.
be of use in further evaluating the presence of statistically equivocal trends such as the USPRS correlation with the WUSPI. Further evaluation of the magnitude of difference in shoulder pain between research subjects and its translation to functional limitations could also be conducted. It would also be interesting to perform the US examination in both upper extremities of all individuals to see whether the dominant extremity is more affected. There is evidence for internal consistency in the USPRS because of correlations between US findings obtained by the single examiner, but it would have been ideal to use multiple equally experienced ultrasonographers examining the same shoulders. This was not possible in the National Veterans’ Wheelchair Games setting. Similarly, it would have been ideal to have multiple physicians use the PESS on each subject to obtain internal consistency data. There is no previously developed criterion standard that can be used for the evaluation of the USPRS and PESS. It is difficult to comment on the sensitivity or specificity of individual scale items because the scale and the method of grading pathology within the scale are newly developed; this is certainly a direction of future investigation. Office-based US has evidence for use in a research and clinical setting to complement the PE and investigate complaints of pain in the shoulder. The USPRS has numerous potential research applications including using the USPRS to measure the long-term effects of new wheelchair designs, specific techniques for wheelchair propulsion, transfer techniques, and epidemiologic investigations. US allows for dynamic evaluations of the shoulder, which is a great advantage over other imaging techniques. US has been used to examine shoulder structures not quantified in the USPRS such as the labrum and teres minor.26,27,44 Development of the USPRS to include such additional structures may be indicated as the utility of this scale is further elucidated. Further investigation into similar methods of quantifying pathology in these structures may be indicated. CONCLUSIONS US is a noninvasive, portable imaging modality with clear advantages for the evaluation of shoulder pathology. The USPRS was developed as a means of quantifying shoulder pathology using US of the shoulder and can be used to evaluate the presence and severity of specific shoulder pathologies. It holds promise as a research tool. The PESS holds promise for following and quantifying subject-reported complaints of shoulder pain in the manual wheelchair user with SCI. The scale has clear potential for use in rehabilitation research. It may also be used in the clinical setting to follow complaints of shoulder pain objectively in populations similar to that examined in this study because of its correlation with the WUSPI. Additional research regarding the reliability and different uses for the PESS is indicated. Shoulder pain is a common secondary medical complication associated with chronic SCI. The prevalence of untreated shoulder pain that curtails activity in persons with SCI indicates that they frequently have unaddressed sources of pain. Presenting screening questions for shoulder pain is warranted when obtaining clinical histories. Further investigation of methods to identify and treat shoulder pain and pathology in persons with SCI is warranted. APPENDIX 1: PHYSICAL EXAMINATION OF THE SHOULDER SCALE Each test is scored from 0 to 2, where “0” indicates the sign or symptom of pain is definitely absent, “1” indicates the sign or symptom of pain is equivocally present, and “2” indicates the sign or symptom of pain is definitely present.
2091
APPENDIX 2: ULTRASOUND SHOULDER PATHOLOGY RATING SCALE Biceps Tendinosis/Tendinopathy 0 1 2 3 4 5 6
⫽ ⫽ ⫽ ⫽ ⫽ ⫽ ⫽
Normal fibrillar pattern and echogenicity Mild loss of fibrillar pattern and/or echogenicity Moderate loss of fibrillar pattern and/or echogenicity Complete or near complete loss of fibrillar pattern Clear longitudinal tear Partial rupture Full rupture/absence of tendon
Supraspinatus Tendinosis/Tendinopathy 0 ⫽ Normal fibrillar pattern and echogenicity 1 ⫽ Mild loss of fibrillar pattern and/or echogenicity 2 ⫽ Moderate loss of fibrillar pattern and/or echogenicity Arch Phys Med Rehabil Vol 89, November 2008
2092
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
3 ⫽ Complete or near complete loss of fibrillar pattern 4 ⫽ Clear tear partial thickness 5 ⫽ Clear tear full thickness Greater Tuberosity Cortical Surface 0 1 2 3
⫽ ⫽ ⫽ ⫽
Smooth hyperechoic cortical surface Mild cortical irregularity or hypoechoic surface Moderate cortical irregularity Marked cortical irregularity or pitting
Dynamic Supraspinatus Impingement 0 ⫽ No evidence of impingement: smooth motion without crepitus 1 ⫽ Mild impingement: slight irregularity in motion with or without crepitus 2 ⫽ Moderate impingement: moderate to marked irregularity in motion with or without crepitus/clear tendon contact with acromion 3 ⫽ Marked impingement: lack of full range of motion/greater tuberosity contact with acromion Dynamic Subscapularis/Biceps/Coracoid Impingement 0 ⫽ No evidence of impingement; smooth motion without crepitus 1 ⫽ Mild impingement: slight irregularity in motion with or without crepitus 2 ⫽ Moderate impingement: moderate to marked irregularity in motion with or without crepitus/clear tendon contact with coracoid 3 ⫽ Marked impingement: lack of full range of motion or clear biceps contact with coracoid process References 1. Bayley JC, Cochran TP, Sledge CB. The weight-bearing shoulder: the impingement syndrome in paraplegics. J Bone Joint Surg Am 1987;69:676-8. 2. Silfverskiold J, Waters RL. Shoulder pain and functional disability in spinal cord injury patients. Clin Orthop Relat Res 1991;(272): 141-5. 3. Donovan WH, Kraft GH. Rotator cuff tear versus suprascapular nerve injury: a problem in differential diagnosis. Arch Phys Med Rehabil 1974;55:424-8. 4. Waring WP, Maynard FM. Shoulder pain in acute traumatic quadriplegia. Paraplegia 1991;29:37-42. 5. Gronley JK, Newsam CJ, Mulroy SJ, Rao SS, Perry J, Helm M. Electromyographic and kinematic analysis of the shoulder during four activities of daily living in men with C6 tetraplegia. J Rehabil Res Dev 2000;37:423-32. 6. Dyson-Hudson TA, Kirshblum SC. Shoulder pain in chronic spinal cord injury, part I: epidemiology, etiology, and pathomechanics. J Spinal Cord Med 2004;27:4-17. 7. Boninger ML, Dicianno BE, Cooper RA, Towers JD, Koontz AM, Souza AL. Shoulder MRI abnormalities, wheelchair propulsion, and gender. Arch Phys Med Rehabil 2003;84:1615-20. 8. Curtis K, Drysdale G, Lanza R, Kolber M, Vitolo R, West R. Shoulder pain in wheelchair users with tetraplegia and paraplegia. Arch Phys Med Rehabil 1999;80:453-7. 9. 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;12:179-86. 10. Nichols PJ, Norman PA, Ennis JR. Wheelchair user’s shoulder? shoulder pain in patients with spinal cord lesions. Scand J Rehabil Med 1979;11:29-32. 11. Pentland WE, Twomey LT. The weight-bearing upper extremity in women with long term paraplegia. Paraplegia 1991;29: 521-30. Arch Phys Med Rehabil Vol 89, November 2008
12. Sie IH, Waters RL, Adkins RH, Gellman H. Upper extremity pain in the postrehabilitation spinal cord injured patient. Arch Phys Med Rehabil 1992;73:44-8. 13. Escobedo EM, Hunter JC, Hollister MC, Patten RM, Goldstein B. MR imaging of rotator cuff tears in individuals with paraplegia. AJR Am J Roentgenol 1997;168:919-23. 14. Boninger ML, Towers JD, Cooper RA, Dicianno BE, Munin MC. Shoulder imaging abnormalities in individuals with paraplegia. J Rehabil Res Dev 2001;38:401-8. 15. Kivimäki J, Ahoniemi E. Ultrasonographic findings in shoulders of able-bodied, paraplegic and tetraplegic subjects. Spinal Cord 2008;46:50-2. 16. Chhem RK, Kaplan PA, Dussault RG. Ultrasonography of the musculoskeletal system. Radiol Clin North Am 1994;32:27589. 17. Hedtmann A, Fett H. [Ultrasound diagnosis of the rotator cuff] [German]. Orthopade 2002;31:236-46. 18. Hodler J, Terrier B, von Schulthess GK, Fuchs WA. MRI and sonography of the shoulder. Clin Radiol 1991;43:323-7. 19. Iannotti JP, Ciccone J, Buss DD, et al. Accuracy of office-based ultrasonography of the shoulder for the diagnosis of rotator cuff tears. J Bone Joint Surg Am 2005;87:1305-11. 20. Jacobson JA, Lancaster S, Prasad A, van Holsbeeck MT, Craig JG, Kolowich P. Full-thickness and partial-thickness supraspinatus tendon tears: value of US signs in diagnosis. Radiology 2004; 230:234-42. 21. Moosmayer S, Heir S, Smith HJ. Sonography of the rotator cuff in painful shoulders performed without knowledge of clinical information: results from 58 sonographic examinations with surgical correlation. J Clin Ultrasound 2007;35:20-6. 22. Rutten MJ, Maresch BJ, Jager GJ, Blickman JG, van Holsbeeck MT. Ultrasound of the rotator cuff with MRI and anatomic correlation. Eur J Radiol 2007;62:427-36. 23. Teefey SA, Rubin DA, Middleton WD, Hildebolt CF, Leibold RA, Yamaguchi K. Detection and quantification of rotator cuff tears: comparison of ultrasonographic, magnetic resonance imaging, and arthroscopic findings in seventy-one consecutive cases. J Bone Joint Surg Am 2004;86-A:708-16. 24. Ziegler DW. The use of in-office, orthopaedist-performed ultrasound of the shoulder to evaluate and manage rotator cuff disorders. J Shoulder Elbow Surg 2004;13:291-7. 25. Moosmayer S, Smith HJ. Diagnostic ultrasound of the shoulder: a method for experts only? Results from an orthopedic surgeon with relative inexpensive compared to operative findings. Acta Orthop 2005;76:503-8. 26. Churchill RS, Fehringer EV, Dubinsky TJ, Matsen FA III. Rotator cuff ultrasonography: diagnostic capabilities. J Am Acad Orthop Surg 2004;12:6-11. 27. Zehetgruber H, Lang T, Wurnig C. Distinction between supraspinatus, infraspinatus and subscapularis tendon tears with ultrasound in 332 surgically confirmed cases. Ultrasound Med Biol 2002;28:711-7. 28. Curtis KA, Roach KE, Applegate EB, et al. Development of the Wheelchair User’s shoulder Pain Index (WUSPI). Paraplegia 1995;33:290-3. 29. Curtis KA, Roach KE, Applegate EB, et al. Reliability and validity of the Wheelchair User’s Shoulder Pain Index (WUSPI). Paraplegia 1995;33:595-601. 30. Hawkins RJ, Kennedy JC. Impingement syndrome in athletes. Am J Sports Med 1980;8:151-8. 31. Neer CS, Welsh RP. The shoulder in sports. Orthop Clin North Am 1977;8:583-91. 32. O’Brien SJ, Pagnani MJ, Fealy S, McGlynn SR, Wilson JB. The active compression test: a new and effective test for diagnosing labral tears and acromioclavicular joint abnormality. Am J Sports Med 1998;26:610-3.
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
33. Park HB, Yokota A, Gill HS, El Rassi G, McFarland EG. Diagnostic accuracy of clinical tests for the different degrees of subacromial impingement syndrome. J Bone Joint Surg Am 2005;87:1446-55. 34. Stetson WB, Templin K. The crank test, the O’Brien test, and routine magnetic resonance imaging scans in the diagnosis of labral tears. Am J Sports Med 2002;30:806-9. 35. Yamaguchi K, Ditsios K, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA. The demographic and morphological features of rotator cuff disease: a comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am 2006;88:1699-704. 36. Gschwend N, Ivosevic-Radovanovic D, Patte D. Rotator cuff tear: relationship between clinical and anatomopathological findings. Arch Orthop Trauma Surg 1988;107:7-15. 37. Gill HS, El Rassi G, Bahk MS, Castillo RC, McFarland EG. Physical examination for partial tears of the biceps tendon. Am J Sports Med 2007;35:1334-40. 38. Schibany N, Zehetgruber H, Kainberger F, et al. Rotator cuff tears in asymptomatic individuals: a clinical and ultrasonographic screening study. Eur J Radiol 2004;51:263-8. 39. Soifer TB, Levy HJ, Soifer FM, Kleinbart F, Vigorita V, Bryk E. Neurohistology of the subacromial space. Arthroscopy 1996;12:182-6.
2093
40. Gotoh M, Hamada K, Yamakawa H, Inoue A, Fukuda H. Increased substance P in subacromial bursa and shoulder pain in rotator cuff diseases. J Orthop Res 1998;16:618-21. 41. Gotoh M, Hamada K, Yamakawa H, et al. Interleukin-1-induced subacromial synovitis and shoulder pain in rotator cuff diseases. Rheumatology (Oxford) 2001;40:995-1001. 42. Gotoh M, Hamada K, Yamakawa H, et al. Interleukin-1-induced glenohumeral synovitis and shoulder pain in rotator cuff diseases. J Orthop Res 2002;20:1365-71. 43. Yanagisawa K, Hamada K, Gotoh M, et al. Vascular endothelial growth factor (VEGF) expression in the subacromial bursa is increased in patients with impingement syndrome. J Orthop Res 2001;19:448-55. 44. Iagnocco A, Coari G, Leone A, Valesini G. Sonographic study of painful shoulder. Clin Exp Rheumatol 2003;21:355-8. Suppliers a. Dynamic Imaging Ltd, 9 Cochrane Sq, Brucefield Industrial Park, Livingston, EH54 9DR UK. b. Version 14; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.
Arch Phys Med Rehabil Vol 89, November 2008
ORIGINAL ARTICLE
Shoulder Ultrasound Abnormalities, Physical Examination Findings, and Pain in Manual Wheelchair Users With Spinal Cord Injury Steven W. Brose, DO, Michael L. Boninger, MD, Bradley Fullerton, MD, Thane McCann, MD, Jennifer L. Collinger, BSE, Bradley G. Impink, BSE, Trevor A. Dyson-Hudson, MD ABSTRACT. Brose SW, Boninger ML, Fullerton B, McCann T, Collinger JL, Impink BG, Dyson-Hudson TA. Shoulder ultrasound abnormalities, physical examination findings, and pain in manual wheelchair users with spinal cord injury. Arch Phys Med Rehabil 2008;89:2086-93. Objectives: To investigate the presence of ultrasound (US) abnormalities in manual wheelchair users with spinal cord injury (SCI) using a quantitative Ultrasound Shoulder Pathology Rating Scale (USPRS). To investigate physical examination (PE) findings using a quantitative Physical Examination of the Shoulder Scale (PESS), and to obtain data about pain and other subject characteristics such as age, years with SCI, and weight. Design: Case series. Setting: National Veterans’ Wheelchair Games 2005 and 2006. Participants: Volunteer sample of manual wheelchair users with SCI participating in the National Veterans’ Wheelchair Games. Interventions: Not applicable. Main Outcome Measures: Presence of relationships between US findings, PE findings, pain, and subject characteristics. Results: The USPRS correlated with age, duration of SCI, and weight (all P⬍.01), and showed a positive trend with the total Wheelchair User’s Shoulder Pain Index (WUSPI) score (r⫽.258, P⫽.073). Several US findings related to presence of PE findings for specific structures. The PESS score correlated with the WUSPI (r⫽.679, P⬍.001) and duration of SCI (P⬍.05). The presence of untreated shoulder pain that curtailed activity was noted in 24.5% of subjects, and this was related to increased WUSPI scores (P⫽.002).
From the Department of Physical Medicine and Rehabilitation, University of Pittsburgh Medical Center, Pittsburgh, PA (Brose, Boninger, Collinger); Human Engineering Research Laboratories, Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, PA (Boninger, Collinger, Impink); The Patient-Physician Partnership, Austin, TX (Fullerton); Children’s Hospital of Austin, Austin, TX (Fullerton); Department of Orthopaedics and Rehabilitation, Walter Reed Army Medical Center, Washington, DC (McCann); Thomas Jefferson University, Philadelphia, PA (McCann); Spinal Cord Injury Research, Kessler Medical Rehabilitation Research and Education Center, West Orange, NJ (Dyson-Hudson); Department of Physical Medicine and Rehabilitation, University of Medicine and Dentistry of New Jersey, New Jersey Medical School, Newark, NJ (Dyson-Hudson). Supported by the Veterans Affairs Center of Excellence for Wheelchairs and Associated Rehabilitation (grant no. B3142C), the National Science Foundation (grant no. DGE0333420), the National Institute on Disability and Rehabilitation (grant no. H133N000019), and the Paralyzed Veterans of America. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Reprint requests to Steven W. Brose, DO, Dept of Physical Medicine and Rehabilitation, University of Pittsburgh Medical Center, 3471 Fifth Ave, Ste 201, Pittsburgh PA 15213, e-mail: [email protected]. 0003-9993/08/8911-00154$34.00/0 doi:10.1016/j.apmr.2008.05.015
Arch Phys Med Rehabil Vol 89, November 2008
Conclusions: PE and US abnormalities are common in manual wheelchair users with SCI. The USPRS and PESS demonstrated evidence for external validity and hold promise as research tools. Untreated shoulder pain is common in manual wheelchair users with SCI, and further investigation of this pain is indicated. Key Words: Rehabilitation; Shoulder; Spinal cord injuries; Ultrasonography; Wheelchairs. © 2008 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation ANUAL WHEELCHAIR USERS have increased demands placed on the structures of the shoulder. In addiM tion to neuropathic phenomena, many factors contribute to mechanical shoulder stress. Activities such as transferring the wheelchair in and out of vehicles, bathing, and even dressing contribute to stress on the shoulders. The mechanical forces created by increased intra-articular pressure and repetitive motions necessitated by manual wheelchair mobility are believed to contribute to the development of shoulder pain, impingement syndromes, and rotator cuff injuries.1,2 Weakness in specific muscles can cause an imbalance in the forces placed on the rotator cuff as well as lead to shortening of antagonists to weak muscles.3,4 Another proposed source of increased demand on the shoulders is overuse of structures that compensate for weakness in other muscle groups.4 Persons with tetraplegia use alternative muscle groups for the lost contribution of the normative primary movers for a given task; an example of this phenomenon would be a person with C6 tetraplegia performing inferior reach. This leads to compensatory use of rotator cuff muscles to perform the task previously accomplished by prime movers.5 Established risk factors for shoulder pain in persons with SCI include increased body mass index, duration of injury, and age.6 Investigations have been conducted to identify ways of reducing shoulder related complaints in the wheelchair-using population. Examples of this include identifying which wheelchair propulsion techniques may contribute to progression of shoulder pathology7 and improving wheelchair design. Despite
List of Abbreviations AC MRI PE PESS SCI US USPRS WUSPI
acromioclavicular magnetic resonance imaging physical examination physical examination of the shoulder scale spinal cord injury ultrasound ultrasound shoulder pathology rating scale Wheelchair User’s Shoulder Pain Index
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
the increasing amount of literature in the field, shoulder pain remains common among persons with SCI who use manual wheelchairs, with reported occurrence ranging from 51% to 78%.1,2,4,8-12 Bayley et al1 found a 30% incidence of chronic, persistent shoulder pain during transfers in a cohort of 94 patients with paraplegia. The most common diagnosis in this group was impingement syndrome with subacromial bursitis. Shoulder pathology in persons with SCI is common. Bayley1 found that 65% of subjects with paraplegia who had signs and symptoms of impingement had tears of the rotator cuff. Escobedo et al13 found that 57% of persons with paraplegia had rotator cuff tears and found a significantly higher rate of rotator cuff tear in persons with paraplegia than in uninjured people. A wide variety of other shoulder pathologies have been described by Boninger et al14 in individuals with paraplegia including acromioclavicular joint abnormalities, coracoacromial ligament thickening and edema, subacromial spurs, and distal clavicle osteolysis. Kivimäki and Ahoniemi15 used diagnostic US to demonstrate that the shoulders of persons with SCI have an increased frequency of irregularity and effusion in the glenohumeral joint space compared with individuals without SCI. Given the frequent occurrence of shoulder pain and pathology in persons with SCI, it is important for both clinical and research purposes to have versatile and inexpensive diagnostic technologies available to evaluate shoulder pathology. The accuracy of office-based ultrasonography has been demonstrated compared with MRI for diagnosing shoulder pathology.3,16-24 Iannotti et al19 found that US correctly diagnosed 88% of full thickness rotator cuff tears compared with 95% accuracy of diagnosis with MRI. Partial thickness tears had been diagnosed with 70% accuracy using US compared with 73% using MRI. US was more accurate than MRI in identifying uninjured shoulders, with an accuracy of 80% for US versus 75% for MRI. The utility of individual US signs and maneuvers for evaluating pathology has been examined in individuals without SCI. Jacobson et al20 documented that tendon nonvisualization was 24% sensitive and 100% specific for supraspinatus tear compared with arthroscopy. To obtain the most accurate assessment of pathology, evaluating a combination of US abnormalities has been recommended as opposed to relying on a single sentinel sign.16,20 By combining the signs of cortical surface irregularity and joint fluid presence, Jacobson20 obtained a sensitivity of 60% and specificity of 100% for the diagnosis of supraspinatus tendon tear. US has the advantages of being easy to perform in an office setting, having a low cost of examination, and allowing dynamic examination of joints during motion. The argument of a steep learning curve is sometimes made against the use of US, but there is evidence indicating that a relatively inexperienced ultrasonographer can still obtain accurate results in US of the shoulder.25 The purpose of this study was to investigate the association between shoulder US abnormalities, shoulder pain, subject characteristics, and physical examination findings in a cohort of manual wheelchair– using persons with SCI. We hypothesized that there would be relationships between increasing US scores for pathology, positive physical examination findings, shoulder pain intensity, and subject characteristics associated with rotator cuff pathology such as increasing age, weight, and duration of SCI. To date, no quantitative scale has been developed to evaluate and quantify shoulder pathology using US. To evaluate our hypothesis, a USPRS was developed for this study as a method of quantifying the results of a series of established clinical tests designed to identify shoulder pathology. The scale was developed using known US findings for normative shoulders and common signs of pathology.16,17,19,20,22-27 Further-
2087
more, because no scale for quantifying physical examination abnormalities has been developed to date, we created a physical examination of the shoulder scale to quantify common clinical tests to evaluate shoulder pain. There is no previously developed criterion standard that can be used to evaluate these scales. This article describes the USPRS and PESS and relationships between US findings, physical examination findings, pain, and self-reported subject characteristics. METHODS Subjects A convenience sample of manual wheelchair users with SCI participating in the National Veterans’ Wheelchair Games in 2005 and 2006 was recruited. Subjects were included in the study if they had injury to the spinal cord, used a manual wheelchair as their primary means of mobility, and were between 18 and 65 years of age. Subjects were excluded from study participation if they had a history of traumatic injury to both their upper extremities that limited mobility, or an upperextremity injury that they had otherwise not recovered from. All subjects provided written informed consent before being included in the study in accordance with procedures approved by the institutional review board. Questionnaires Shoulder pain was measured using the WUSPI.28,29 The WUSPI is a 15-item, self-report instrument that provides a personal estimate of shoulder pain experienced during transfers, wheelchair mobility, self-care, and other general activities. Each item is scored using a continuous 10-cm visual analog scale that is anchored at the ends with 0 (no pain) and 10 (worst pain ever experienced). Individual item scores are summed to arrive at a total index score, which ranges from 0 to 150. Each subject also filled out a questionnaire including information about their specific injury, general characteristics such as age and weight, and specific questions regarding the nature of their shoulder pain. All information including level and completeness of SCI was self-reported by using this questionnaire. Physical Examination The PESS score was obtained by performing a series of 11 commonly used physical examination maneuvers for shoulder pathology. The PESS consisted of the following maneuvers: (1) palpation over the bicipital groove/biceps tendon, (2) palpation over the greater tuberosity/supraspinatus tendon, (3) palpation over the acromioclavicular joint, (4) Neer sign, (5) Hawkins-Kennedy impingement sign, (6) painful arc, (7) supraspinatus (Jobe’s or “empty can”) test, (8) resisted external rotation, (9) resisted internal rotation; and the active compression (O’Brien) test for the (10) labrum and (11) AC joint. The Neer, O’Brien, and Hawkins-Kennedy tests were performed as described in the original publications.30-32 The O’Brien tests for the labrum and AC joint were treated as separate tests, because it was noted that some individuals had positive findings on both tests, and hence the 2 parts of this test were scored as separate tests within the PESS. The individual scores of PE tests (appendix 1) were added together to form the PESS for a shoulder. The maximum possible score for a shoulder was 22, and the minimum was 0. The tests were chosen because of their common clinical usage and also because their validity has been investigated previously.33,34 The PESS was performed on both shoulders of each subject by one of several trained physician examiners. The examiners Arch Phys Med Rehabil Vol 89, November 2008
2088
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
finding or characteristic was related to the score in a variable such as the PESS or USPRS, dichotomizations were performed. Some examples of dichotomizations included the presence or absence of untreated shoulder pain, the presence of positive findings in specific clinical tests making up the PESS, the presence of tetraplegia, and the occurrence of complete injury. Differences between dichotomized groups were investigated using a Mann-Whitney U test for nonparametric variable comparison, and a t test for independent samples was used for normally distributed variable analysis. RESULTS
Fig 1. Marked cortical irregularity. Grade 3 on USPRS.
were blind to the results of the questionnaire and WUSPI. All physical examinations were performed with the test subject seated in a wheelchair. US Examination Each participant had US evaluation of a single shoulder. The nondominant side was tested provided there was no prior traumatic injury to the extremity. A single experienced examiner performed all US examinations. The examiner was blind to the results of the questionnaire, WUSPI, and physical examination. A Diasus US Machinea with a transducer 8 to 16MHz was used to collect images. All US examinations were performed with the test subject seated in a wheelchair. The USPRS is a scale based on 5 US signs; 3 signs are static and 2 are dynamic. The static tests were greater tuberosity cortical surface irregularity, supraspinatus tendinopathy, and bicipital tendinopathy. The dynamic tests were supraspinatus impingement and subscapularis/biceps/coracoid impingement. Commonly used signs of pathology on US16,17,19,20,22-27 determined type and degree of pathology. Examples of signs of pathology may include loss of fibrillar pattern for tendinopathy, regions of lucency for a tear, and uneven motion for impingement. A simple ordinal rating scale similar to that used for muscle strength testing was applied to each US sign based on the amount of pathology present. All the scores were summed to form the USPRS for a given shoulder (appendix 2). Figures 1 and 2 provide examples of how to score the USPRS for 2 pathologies. Data Analysis All data analysis was performed using SPSS.b Descriptive analysis was conducted on all variables analyzed for statistical relationships. All correlations were investigated by obtaining the nonparametric Spearman . Correlations between the WUSPI, USPRS, PESS, age, weight, and years with SCI were investigated. To analyze whether the presence or absence of a Arch Phys Med Rehabil Vol 89, November 2008
Subject Characteristics Forty-nine subjects with chronic SCI who used manual wheelchairs as their primary means of mobility participated in the study. The mean subject age ⫾ SD was 44.8⫾9.2 years, and 48 of the 49 individuals who participated in the study were men, which was representative of the participants in the National Veterans’ Wheelchair Games. The average duration with SCI was 16.35⫾9.3 years, and the median was 15.9 years. Average weight was 187.69⫾46.4lb, and the median was 185lb. Complete injuries were reported by 46.9% of subjects (n⫽23), 46.9% had an incomplete injury (n⫽23), and 6.1% were unspecified (n⫽3). Persons with tetraplegia made up 28.6% of the study population (n⫽14), 67.3% had paraplegia (n⫽33), and 4.1% were unspecified (n⫽2). Sixty-seven percent of subjects reported shoulder pain in the last month. Nearly one quarter of the subjects (24.5%) had untreated shoulder pain that curtailed their activity. The only normally distributed variables in this study were height, weight, age, and years with SCI. The USPRS had a Kolmogorov-Smirnov value that indicated it may be normally distributed (.354), but because it is a continuous variable, it was analyzed using nonparametric testing. WUSPI Scores Table 1 displays correlations between the WUSPI, PESS, USPRS, and other variables. Eighty-four percent of subjects
Fig 2. Partial-thickness tear of the supraspinatus tendon. Grade 4 on USPRS.
2089
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose Table 1: Correlations and Statistical Relationships
Scales
USPRS PESS-both shoulders combined WUSPI
Age
Weight
Years With SCI
rs⫽417 P⫽.003* rs⫽.265 P⫽.072 rs⫽.242 P⫽.095
rs⫽.468 P⫽.001* rs⫽.151 P⫽.311 rs⫽.328 P⫽.021*
rs⫽.368 P⫽.009* rs⫽.328 P⫽.024* rs⫽.304 P⫽.034*
Presence of Untreated Shoulder Pain Curtailing Activity
P⫽.811 P⫽.008* P⫽.003*
WUSPI
rs⫽.258 P⫽.073 rs⫽.697 P⬍.001* NA
PESS-US Examined Shoulder
Presence of Complete Injury
Tetraplegia Versus Paraplegia
rs⫽.247 P⫽.095 NA
P⫽.289
P⫽.215
P⫽.592
P⫽.399
NA
P⫽.866
P⫽.575
Abbreviations: NA, not applicable; rs, Spearman’s rho. *P⬍.05.
reported pain on at least 1 item of the WUSPI, which included any score greater than 0 on any item. The mean WUSPI score was 23.0⫾28.5 out of a possible 150, and the median was 8.4. Recorded subject WUSPI scores ranged from 0 to 109. Individuals reporting elbow or shoulder noise during activity had higher WUSPI scores than those without noise in these joints (P⫽.01). The average WUSPI score among individuals reporting shoulder or elbow noise during activity was 33.7, compared with an average WUSPI score of 16 in individuals not reporting noise. Subjects with untreated shoulder pain curtailing activity were also noted to have higher WUSPI scores. The mean WUSPI score of individuals with untreated shoulder pain curtailing their activity was 40.7, compared with a mean score of 16.2 in individuals who did not report untreated pain curtailing activity. The WUSPI correlated with weight and duration of SCI. No relationship was found between the WUSPI and age, whether the subjects had a complete injury, or the presence of tetraplegia versus paraplegia. Physical Examination The mean PESS score, which was the sum of the 11 physical examination scores for both shoulders combined, was 8.98⫾9.69 out of a possible 44 points, and the median was 5. Recorded scores ranged from 0 to 36 points. Figure 3 details the frequencies of positive findings for the 11 physical examination tests making up the PESS. Individuals with shoulder pain in the last month had higher PESS scores than those without pain. The mean PESS score in subjects reporting pain in the last month was 11.1, compared with a PESS score of 4.4 in individuals without shoulder pain in the last month. Individuals with untreated shoulder pain that curtailed their activity also had higher PESS scores (P⫽.008). The mean PESS score in individuals with untreated shoulder pain curtailing activity was 14.6, compared with a PESS score of 6.8 for individuals who did not have untreated shoulder pain curtailing activity. The PESS correlated with the WUSPI and duration of SCI. There was no correlation between the PESS and age or weight. The average sum of the 11 physical examination scores of the right shoulders was 1.99 points higher than that of the left shoulders. The sum of the 11 physical examination scores of each shoulder correlated with the sum of the 11 physical examination scores of the opposing shoulder (r⫽.498; P⫽.001). US Findings All shoulders examined exhibited abnormalities on US. Figure 4 details the frequencies of the 5 abnormalities making up the USPRS. All 5 measures evaluated on the US examina-
tion positively correlated with each other (P⬍.05). The mean total USPRS score was 6.84⫾3.19 out of a possible 20 with a median of 7. USPRS total scores ranged from 2 to 15 points. The USPRS correlated with age, duration of SCI, and weight, and showed a trend in correlation with the WUSPI that did not reach statistical significance. The USPRS was not significantly correlated with the PESS. Although the USPRS did not correlate with the PESS, increasing pathology of several measures of the USPRS was found to relate to the presence of individual signs in PE. One notable finding was that individuals with tenderness at the supraspinatus/greater tuberosity had higher scores for dynamic supraspinatus impingement than those who did not have tenderness (P⫽.039). Individuals with tenderness at this location also had increased greater tuberosity cortical surface irregularity than those who were not tender (P⫽.03). Increased cortical surface irregularity was noted in individuals with a positive Neer sign (P⫽.027). In the same fashion, the presence of a positive Neer sign was associated with higher degrees of supraspinatus tendinopathy on US (P⫽.019). Subjects with a positive resisted external rotation test had higher scores for dynamic supraspinatus impingement (P⫽.016). There was no identifiable relationship between bicipital tendinopathy and tenderness at the bicipital groove.
Fig 3. Physical examination findings.
Arch Phys Med Rehabil Vol 89, November 2008
2090
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
Fig 4. Ultrasound findings.
DISCUSSION The findings of this study confirmed our hypothesis that increasing shoulder pathology visualized on US would be associated with subject characteristics known to be risk factors for shoulder pathology. Increasing age is a known risk factor for shoulder pathology in the non-SCI population.35 The USPRS has evidence for external validity because of its correlation with age, weight, and duration of SCI. Shoulder pathologies have been described to coexist frequently with one another.34,36 The positive intratest correlation of individual tests making up the USPRS provides some evidence of internal consistency in the USPRS. The association of specific findings on the USPRS with certain clinical tests provides evidence that the examinations chosen to form the USPRS were valid choices. The relationship between cortical irregularity and supraspinatus tenderness is a finding worthy of note, because the cortical irregularity sign on US has previously been described as useful in evaluating supraspinatus tear.20 The prevalence of cortical irregularity of the greater tuberosity on US, supraspinatus impingement on US, and positive supraspinatus physical examination tests in this study indicate that pathology in the supraspinatus may be a frequent problem in individuals with SCI. The lack of an association between bicipital tenderness and bicipital tendinopathy appears to concur with literature noting the low sensitivity and specificity of tenderness at the bicipital groove for bicipital pathology.37 The correlation between the total summed PESS for both shoulders and the WUSPI indicates that the PESS has evidence for external validity and may have use for quantifying painful shoulder pathology. Statistical analysis indicates that a portion of the pain measured by the WUSPI may be related to pathology in the structures tested in this PE sequence. The correlation of each shoulder’s PESS with the opposing shoulder indicates that persons with SCI presenting with unilateral shoulder pathology may in fact have underlying bilateral shoulder pathology. This is a topic that warrants further investigation. The relationship of the PESS to pain in the last month and the correlation with the subject’s duration of SCI is further evidence for external validity of the PESS. Arch Phys Med Rehabil Vol 89, November 2008
Our application of the O’Brien PE maneuver involved scoring each portion of the test as a separate item in the PESS, because some subjects had positive findings for both the acromioclavicular and labral portions of the test. The test is sometimes used clinically to differentiate pathologies between these 2 shoulder structures, as opposed to being treated as 2 separate tests. It is reasonable to treat the O’Brien maneuver for the AC joint and labrum as 2 separately scored items in the PESS because shoulder pathologies frequently coexist with one another.34,36 It is possible to use the O’Brien test to evaluate coexisting AC joint and labral pathology. The relationship between the WUSPI and the presence of shoulder pain that has not been treated by a physician and that is curtailing activity is a noteworthy finding of the study. There is a population of persons with SCI who have untreated shoulder pain. Persons with SCI learn to cope with impairments, and it is possible that clinically significant shoulder pain is underappreciated in this group. Roughly one fourth of our subjects had shoulder pain that limited their activity and was not treated by a physician. This lends credence to the assertion that this untreated shoulder pain is clinically significant and has an impact on quality of life. Further investigation of this phenomenon and the ways that it affects individuals with SCI is warranted. Contrary to our hypothesis, a statistically significant correlation between the USPRS and the WUSPI was not supported by the data, although a trend was identified. A lack of statistically significant correlation of the USPRS with pain is not necessarily unexpected. It has been reported that individuals with pathology affecting multiple tendons or with full-thickness tears may have mild to no pain.36 This is seen with increasing frequency as individuals grow older and has been studied with regard to abnormalities in the supraspinatus tendon,38 and 100% of our subject population had pathology of the supraspinatus tendon. Age was not significantly correlated with the WUSPI. Our findings support the assertion that absence of pain does not represent absence of shoulder pathology, and pain may be a marker for future shoulder pathology even if current pathology is not present; this is a topic for further investigation. Furthermore, although the sensation of pain in impingement syndrome is sometimes assumed to be directly related to pathology of the rotator cuff, there is a complex anatomical proximity of several structures that might be sources of pain. Soifer et al39 found that there was a larger concentration of free nerve fibers in the subacromial bursa than the rotator cuff tendon or biceps tendon. It is believed that the presence of inflammatory cytokines or sensitization of the nerve endings in the bursa may sometimes be responsible for the pain associated with impingement syndrome.40-43 Another factor that may contribute to a lack of statistical relationship between the USPRS and the WUSPI is the broad range of activities in the WUSPI that may involve shoulder structures not visualized with US or not examined in this protocol. It is difficult to visualize the posterior aspects of the supraspinatus and infraspinatus, as well as the glenoid labrum. A lack of correlation between the total scores of the USPRS and the PESS is not surprising because a number of tests in the physical examination evaluate structures not represented in the USPRS. Study Limitations Limitations of the study include the selection of a subject population predominantly composed of men participating in athletic events. Further study is needed to determine whether the findings of this study may be generalized to populations broader than this. Although the sample size of 49 subjects was large enough to obtain useful information, a larger sample may
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
(1)
Biceps tendon/bicipital groove tenderness. Palpation of the biceps tendon and bicipital groove is best achieved with the arm in 10° of internal rotation. (2) Supraspinatus tendon/greater tuberosity tenderness. Palpation of the greater tuberosity and supraspinatus insertion is best achieved by slightly extending and internally rotating the arm. The greater tuberosity can be found distal to the anterolateral border of the acromion. (3) Acromioclavicular joint tenderness. Pain with palpation of the acromioclavicular joint. (4) Resisted external, and (5) internal rotation. The subject isometrically attempts rotation against resistance while keeping the palm facing medially and elbow flexed at 90°. (6) Supraspinatus test. Resistance is applied with the patient’s arm abducted to 90°, forward-flexed to 30°, and pronated. The test is positive if pain or weakness is present during resistance. (7) Painful Arc Test. Pain between 60° and 120° of active shoulder abduction in the coronal plane. (8) Neer impingement sign. With the examiner’s opposite hand on the trapezius, the patient’s arm is forcibly elevated through forward flexion by the examiner, causing a jamming of the greater tuberosity against the anterioinferior border of the acromion. The test is positive if it produces pain. (9) Hawkins-Kennedy impingement sign. Slightly flexed at the elbow, the patient’s arm is first elevated forward to 90° and then forcibly medially rotated. This pushes the supraspinatus tendon against the anterior surface of the coracoacromial ligament. The test is positive if the maneuver produces pain. (10) O’Brien Active Compression Test for Acromioclavicular Joint Pathology and (11) Labral Pathology. While seated, the patient is asked to forward-flex the affected arm to 90° with the elbow in full extension. The patient then adducts the arm 10° to 15° medial to the sagittal plane of the body and fully pronates the arm so the thumb points downward; the examiner, standing behind the patient, then applies a downward force to the arm; the maneuver is repeated with the palm fully supinated. The test is positive if pain is elicited during the first maneuver and reduced or eliminated during the second maneuver. The test for acromioclavicular joint is positive if the test elicits pain localized to that location, and the test is positive for the labrum if there is pain or painful clicking described deep within the shoulder.
be of use in further evaluating the presence of statistically equivocal trends such as the USPRS correlation with the WUSPI. Further evaluation of the magnitude of difference in shoulder pain between research subjects and its translation to functional limitations could also be conducted. It would also be interesting to perform the US examination in both upper extremities of all individuals to see whether the dominant extremity is more affected. There is evidence for internal consistency in the USPRS because of correlations between US findings obtained by the single examiner, but it would have been ideal to use multiple equally experienced ultrasonographers examining the same shoulders. This was not possible in the National Veterans’ Wheelchair Games setting. Similarly, it would have been ideal to have multiple physicians use the PESS on each subject to obtain internal consistency data. There is no previously developed criterion standard that can be used for the evaluation of the USPRS and PESS. It is difficult to comment on the sensitivity or specificity of individual scale items because the scale and the method of grading pathology within the scale are newly developed; this is certainly a direction of future investigation. Office-based US has evidence for use in a research and clinical setting to complement the PE and investigate complaints of pain in the shoulder. The USPRS has numerous potential research applications including using the USPRS to measure the long-term effects of new wheelchair designs, specific techniques for wheelchair propulsion, transfer techniques, and epidemiologic investigations. US allows for dynamic evaluations of the shoulder, which is a great advantage over other imaging techniques. US has been used to examine shoulder structures not quantified in the USPRS such as the labrum and teres minor.26,27,44 Development of the USPRS to include such additional structures may be indicated as the utility of this scale is further elucidated. Further investigation into similar methods of quantifying pathology in these structures may be indicated. CONCLUSIONS US is a noninvasive, portable imaging modality with clear advantages for the evaluation of shoulder pathology. The USPRS was developed as a means of quantifying shoulder pathology using US of the shoulder and can be used to evaluate the presence and severity of specific shoulder pathologies. It holds promise as a research tool. The PESS holds promise for following and quantifying subject-reported complaints of shoulder pain in the manual wheelchair user with SCI. The scale has clear potential for use in rehabilitation research. It may also be used in the clinical setting to follow complaints of shoulder pain objectively in populations similar to that examined in this study because of its correlation with the WUSPI. Additional research regarding the reliability and different uses for the PESS is indicated. Shoulder pain is a common secondary medical complication associated with chronic SCI. The prevalence of untreated shoulder pain that curtails activity in persons with SCI indicates that they frequently have unaddressed sources of pain. Presenting screening questions for shoulder pain is warranted when obtaining clinical histories. Further investigation of methods to identify and treat shoulder pain and pathology in persons with SCI is warranted. APPENDIX 1: PHYSICAL EXAMINATION OF THE SHOULDER SCALE Each test is scored from 0 to 2, where “0” indicates the sign or symptom of pain is definitely absent, “1” indicates the sign or symptom of pain is equivocally present, and “2” indicates the sign or symptom of pain is definitely present.
2091
APPENDIX 2: ULTRASOUND SHOULDER PATHOLOGY RATING SCALE Biceps Tendinosis/Tendinopathy 0 1 2 3 4 5 6
⫽ ⫽ ⫽ ⫽ ⫽ ⫽ ⫽
Normal fibrillar pattern and echogenicity Mild loss of fibrillar pattern and/or echogenicity Moderate loss of fibrillar pattern and/or echogenicity Complete or near complete loss of fibrillar pattern Clear longitudinal tear Partial rupture Full rupture/absence of tendon
Supraspinatus Tendinosis/Tendinopathy 0 ⫽ Normal fibrillar pattern and echogenicity 1 ⫽ Mild loss of fibrillar pattern and/or echogenicity 2 ⫽ Moderate loss of fibrillar pattern and/or echogenicity Arch Phys Med Rehabil Vol 89, November 2008
2092
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
3 ⫽ Complete or near complete loss of fibrillar pattern 4 ⫽ Clear tear partial thickness 5 ⫽ Clear tear full thickness Greater Tuberosity Cortical Surface 0 1 2 3
⫽ ⫽ ⫽ ⫽
Smooth hyperechoic cortical surface Mild cortical irregularity or hypoechoic surface Moderate cortical irregularity Marked cortical irregularity or pitting
Dynamic Supraspinatus Impingement 0 ⫽ No evidence of impingement: smooth motion without crepitus 1 ⫽ Mild impingement: slight irregularity in motion with or without crepitus 2 ⫽ Moderate impingement: moderate to marked irregularity in motion with or without crepitus/clear tendon contact with acromion 3 ⫽ Marked impingement: lack of full range of motion/greater tuberosity contact with acromion Dynamic Subscapularis/Biceps/Coracoid Impingement 0 ⫽ No evidence of impingement; smooth motion without crepitus 1 ⫽ Mild impingement: slight irregularity in motion with or without crepitus 2 ⫽ Moderate impingement: moderate to marked irregularity in motion with or without crepitus/clear tendon contact with coracoid 3 ⫽ Marked impingement: lack of full range of motion or clear biceps contact with coracoid process References 1. Bayley JC, Cochran TP, Sledge CB. The weight-bearing shoulder: the impingement syndrome in paraplegics. J Bone Joint Surg Am 1987;69:676-8. 2. Silfverskiold J, Waters RL. Shoulder pain and functional disability in spinal cord injury patients. Clin Orthop Relat Res 1991;(272): 141-5. 3. Donovan WH, Kraft GH. Rotator cuff tear versus suprascapular nerve injury: a problem in differential diagnosis. Arch Phys Med Rehabil 1974;55:424-8. 4. Waring WP, Maynard FM. Shoulder pain in acute traumatic quadriplegia. Paraplegia 1991;29:37-42. 5. Gronley JK, Newsam CJ, Mulroy SJ, Rao SS, Perry J, Helm M. Electromyographic and kinematic analysis of the shoulder during four activities of daily living in men with C6 tetraplegia. J Rehabil Res Dev 2000;37:423-32. 6. Dyson-Hudson TA, Kirshblum SC. Shoulder pain in chronic spinal cord injury, part I: epidemiology, etiology, and pathomechanics. J Spinal Cord Med 2004;27:4-17. 7. Boninger ML, Dicianno BE, Cooper RA, Towers JD, Koontz AM, Souza AL. Shoulder MRI abnormalities, wheelchair propulsion, and gender. Arch Phys Med Rehabil 2003;84:1615-20. 8. Curtis K, Drysdale G, Lanza R, Kolber M, Vitolo R, West R. Shoulder pain in wheelchair users with tetraplegia and paraplegia. Arch Phys Med Rehabil 1999;80:453-7. 9. 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;12:179-86. 10. Nichols PJ, Norman PA, Ennis JR. Wheelchair user’s shoulder? shoulder pain in patients with spinal cord lesions. Scand J Rehabil Med 1979;11:29-32. 11. Pentland WE, Twomey LT. The weight-bearing upper extremity in women with long term paraplegia. Paraplegia 1991;29: 521-30. Arch Phys Med Rehabil Vol 89, November 2008
12. Sie IH, Waters RL, Adkins RH, Gellman H. Upper extremity pain in the postrehabilitation spinal cord injured patient. Arch Phys Med Rehabil 1992;73:44-8. 13. Escobedo EM, Hunter JC, Hollister MC, Patten RM, Goldstein B. MR imaging of rotator cuff tears in individuals with paraplegia. AJR Am J Roentgenol 1997;168:919-23. 14. Boninger ML, Towers JD, Cooper RA, Dicianno BE, Munin MC. Shoulder imaging abnormalities in individuals with paraplegia. J Rehabil Res Dev 2001;38:401-8. 15. Kivimäki J, Ahoniemi E. Ultrasonographic findings in shoulders of able-bodied, paraplegic and tetraplegic subjects. Spinal Cord 2008;46:50-2. 16. Chhem RK, Kaplan PA, Dussault RG. Ultrasonography of the musculoskeletal system. Radiol Clin North Am 1994;32:27589. 17. Hedtmann A, Fett H. [Ultrasound diagnosis of the rotator cuff] [German]. Orthopade 2002;31:236-46. 18. Hodler J, Terrier B, von Schulthess GK, Fuchs WA. MRI and sonography of the shoulder. Clin Radiol 1991;43:323-7. 19. Iannotti JP, Ciccone J, Buss DD, et al. Accuracy of office-based ultrasonography of the shoulder for the diagnosis of rotator cuff tears. J Bone Joint Surg Am 2005;87:1305-11. 20. Jacobson JA, Lancaster S, Prasad A, van Holsbeeck MT, Craig JG, Kolowich P. Full-thickness and partial-thickness supraspinatus tendon tears: value of US signs in diagnosis. Radiology 2004; 230:234-42. 21. Moosmayer S, Heir S, Smith HJ. Sonography of the rotator cuff in painful shoulders performed without knowledge of clinical information: results from 58 sonographic examinations with surgical correlation. J Clin Ultrasound 2007;35:20-6. 22. Rutten MJ, Maresch BJ, Jager GJ, Blickman JG, van Holsbeeck MT. Ultrasound of the rotator cuff with MRI and anatomic correlation. Eur J Radiol 2007;62:427-36. 23. Teefey SA, Rubin DA, Middleton WD, Hildebolt CF, Leibold RA, Yamaguchi K. Detection and quantification of rotator cuff tears: comparison of ultrasonographic, magnetic resonance imaging, and arthroscopic findings in seventy-one consecutive cases. J Bone Joint Surg Am 2004;86-A:708-16. 24. Ziegler DW. The use of in-office, orthopaedist-performed ultrasound of the shoulder to evaluate and manage rotator cuff disorders. J Shoulder Elbow Surg 2004;13:291-7. 25. Moosmayer S, Smith HJ. Diagnostic ultrasound of the shoulder: a method for experts only? Results from an orthopedic surgeon with relative inexpensive compared to operative findings. Acta Orthop 2005;76:503-8. 26. Churchill RS, Fehringer EV, Dubinsky TJ, Matsen FA III. Rotator cuff ultrasonography: diagnostic capabilities. J Am Acad Orthop Surg 2004;12:6-11. 27. Zehetgruber H, Lang T, Wurnig C. Distinction between supraspinatus, infraspinatus and subscapularis tendon tears with ultrasound in 332 surgically confirmed cases. Ultrasound Med Biol 2002;28:711-7. 28. Curtis KA, Roach KE, Applegate EB, et al. Development of the Wheelchair User’s shoulder Pain Index (WUSPI). Paraplegia 1995;33:290-3. 29. Curtis KA, Roach KE, Applegate EB, et al. Reliability and validity of the Wheelchair User’s Shoulder Pain Index (WUSPI). Paraplegia 1995;33:595-601. 30. Hawkins RJ, Kennedy JC. Impingement syndrome in athletes. Am J Sports Med 1980;8:151-8. 31. Neer CS, Welsh RP. The shoulder in sports. Orthop Clin North Am 1977;8:583-91. 32. O’Brien SJ, Pagnani MJ, Fealy S, McGlynn SR, Wilson JB. The active compression test: a new and effective test for diagnosing labral tears and acromioclavicular joint abnormality. Am J Sports Med 1998;26:610-3.
MANUAL WHEELCHAIR USERS WITH SPINAL CORD INJURY, Brose
33. Park HB, Yokota A, Gill HS, El Rassi G, McFarland EG. Diagnostic accuracy of clinical tests for the different degrees of subacromial impingement syndrome. J Bone Joint Surg Am 2005;87:1446-55. 34. Stetson WB, Templin K. The crank test, the O’Brien test, and routine magnetic resonance imaging scans in the diagnosis of labral tears. Am J Sports Med 2002;30:806-9. 35. Yamaguchi K, Ditsios K, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA. The demographic and morphological features of rotator cuff disease: a comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am 2006;88:1699-704. 36. Gschwend N, Ivosevic-Radovanovic D, Patte D. Rotator cuff tear: relationship between clinical and anatomopathological findings. Arch Orthop Trauma Surg 1988;107:7-15. 37. Gill HS, El Rassi G, Bahk MS, Castillo RC, McFarland EG. Physical examination for partial tears of the biceps tendon. Am J Sports Med 2007;35:1334-40. 38. Schibany N, Zehetgruber H, Kainberger F, et al. Rotator cuff tears in asymptomatic individuals: a clinical and ultrasonographic screening study. Eur J Radiol 2004;51:263-8. 39. Soifer TB, Levy HJ, Soifer FM, Kleinbart F, Vigorita V, Bryk E. Neurohistology of the subacromial space. Arthroscopy 1996;12:182-6.
2093
40. Gotoh M, Hamada K, Yamakawa H, Inoue A, Fukuda H. Increased substance P in subacromial bursa and shoulder pain in rotator cuff diseases. J Orthop Res 1998;16:618-21. 41. Gotoh M, Hamada K, Yamakawa H, et al. Interleukin-1-induced subacromial synovitis and shoulder pain in rotator cuff diseases. Rheumatology (Oxford) 2001;40:995-1001. 42. Gotoh M, Hamada K, Yamakawa H, et al. Interleukin-1-induced glenohumeral synovitis and shoulder pain in rotator cuff diseases. J Orthop Res 2002;20:1365-71. 43. Yanagisawa K, Hamada K, Gotoh M, et al. Vascular endothelial growth factor (VEGF) expression in the subacromial bursa is increased in patients with impingement syndrome. J Orthop Res 2001;19:448-55. 44. Iagnocco A, Coari G, Leone A, Valesini G. Sonographic study of painful shoulder. Clin Exp Rheumatol 2003;21:355-8. Suppliers a. Dynamic Imaging Ltd, 9 Cochrane Sq, Brucefield Industrial Park, Livingston, EH54 9DR UK. b. Version 14; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.
Arch Phys Med Rehabil Vol 89, November 2008