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The Relationship Between Lower Extremity Strength and Shoulder Overuse Symptoms:
A Model Based on Polio Survivors
Mary G. Klein, PhD;1 John Whyte, MD PhD;2'5 Mary Ann Keenan, MD;1'5
Alberto Esquenazi, MD;3'5 Marcia Polansky, ScD4
Philadelphia, PA
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1) Albert Einstein Medical Center; 2) Moss Rehabilitation Research Institute;
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3) MossRehab Hospital; 4) MCP-Hahnemann University;
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5) Temple University School of Medicine
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Supported by grant DAMD17-95-1-5079 from the U.S. Department of the Army.
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Reprint requests to Mary G. Klein, Korman 204-B, Moss Rehabilitation Research
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Institute, 1200 West Tabor Road, Philadelphia, PA 19141; Phone: 215-456-7864,
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FAX: 215-456-9514.
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ABSTRACT
Objective: To determine the relationship between lower extremity weakness and shoulder
26
overuse symptoms among polio survivors. We predicted that individuals with moderate
27
weakness in their leg extensor muscles use their arms to help compensate for this weakness and
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would be at high risk for developing symptoms of shoulder overuse.
29
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Design: A cohort study of polio survivors recruited from the Einstein-Moss Post-Polio
Management Program, the community and the surrounding tri-state area.
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Setting: A research laboratory at Moss Rehabilitation Research Institute.
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Participants: One hundred ninety-four polio survivors were studied; demographic and
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medical history data, symptom data, and strength data were obtained for each.
Main Outcome Measures: Presence or absence of shoulder symptoms and ratings of pain by
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visual analogue scale (VAS) were recorded. Strength was measured using a hand-held
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dynamometer and manual muscle testing (MMT).
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Results: Shoulder symptoms could be grouped into two distinct clusters based on the type of
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testing used for assessment. Symptoms elicited by palpation were present in 26% of the subjects
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and were strongly related to knee extensor strength and weight. These symptoms were more
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common among females than males (42% vs. 10%). Symptoms elicited by resistance tests were
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present in 33% of the subjects and were seen with equal frequency in both genders. These
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symptoms were also related to lower extremity strength, however the specific relationship was
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not as clear as for the palpation-related symptoms.
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Conclusions: Lower extremity weakness predisposes individuals to shoulder overuse
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symptoms. Gender and body weight are contributing factors. These results may generalize to
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other populations with lower extremity weakness, including the elderly.
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INTRODUCTION
The relationship between muscle weakness, overuse and injury is thought to be both a
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cyclical and a reciprocal one. Muscle weakness can produce overuse, overuse can lead to further
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weakness, and both can predispose to injury.1 Overuse can occur directly when weakened
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muscles need to work harder to maintain a certain force or indirectly when alternate muscles are
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recruited to compensate for weak ones. Individuals can enter this weakness--overuse--injury
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cycle at different points and at different levels of weakness.
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There are various etiologies of muscle weakness, but each may lead to overuse. Muscle
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weakness can occur as a result of lack of exercise (disuse), after an injury or illness, or as the
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result of a disease, such as polio. The resulting muscle weakness may be severe or mild. Often,
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individuals may not even be aware of mild muscle weakness. They may function and feel normal
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during their daily activities but might actually be overusing muscles to compensate for
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undetected "subclinical" weakness.
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Because the muscle weakness experienced by many polio survivors is often quite
61
significant, this population is susceptible to an accelerated pattern of overuse. Theoretically, this
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would allow the symptoms of overuse to be readily observed in a small population over a short
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period of time. For this reason, we hypothesize that the post-polio population provides an
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excellent model for the study of overuse disorders in the general population.
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There are over one million polio survivors in the United States.2 After recovering from
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the acute infection, survivors were left with varying degrees of muscle strength. As time passed,
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they became very adept at compensating for weakened muscles, with the end result being a
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higher risk of overuse and trauma to the compensating muscles as well as those muscles
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weakened by the initial polio.
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Although the muscle weakness of the polio survivor is often more pronounced than that
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noted in the general population, polio is not a primary muscle disease. Normal muscle
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physiology, sensation and motor control are preserved.3 It is thus a "pure" model for studying
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the effects of muscle weakness on the remainder of the musculoskeletal system.
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Polio affected the lower extremities with twice the frequency of the upper extremities.4
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As a result, the most common complaints of polio survivors are related to issues of mobility.5
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For example, individuals with knee or hip extensor weakness may have difficulty with activities
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like climbing stairs or rising from a chair and often use their arms to assist with weight-bearing
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(e.g. to push off the armrests of a chair or pull up on a stair railing). We hypothesized that this
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behavior would lead to increased susceptibility to shoulder overuse and there would be an
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association between leg extensor weakness and shoulder overuse symptoms.
81
Previous studies have looked at the relationship of lower extremity weakness to various
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gait parameters and overuse of compensatory muscles in the legs among polio survivors.3'6 There
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have also been studies on upper extremity overuse in individuals with paraplegia who must rely
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exclusively on their upper extremities for mobility.7'8 However, to date, there have not been any
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studies which explored the potential relationship between lower extremity weakness and upper
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extremity overuse in an ambulatory population.
87
Therefore, the objective of this study was to explore the relationship between lower
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extremity weakness and upper extremity overuse among polio survivors, focusing specifically on
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shoulder symptoms and leg extensor strength. We predicted a curvilinear relationship between
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symptoms and strength (i.e. that the proportion of subjects with shoulder symptoms would be
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highest in the mid-range of leg extensor strength). These individuals would be more active than
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those with severe weakness and would put more stress on their arms during everyday activities
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than those with mild or no noticeable weakness. We also predicted that shoulder symptoms
94
would increase with age, weight and activity level and that the duration of time since the original
95
polio infection would also be an important factor.
96
97
METHOD
98
Subjects
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A total of 290 polio survivors were recruited from the Einstein-Moss Post-Polio
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Management Program and the community at large, including the surrounding four-state area:
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Pennsylvania, New Jersey, Delaware, and southern New York. The inclusion criteria were as
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follows: 1) a history of polio, 2) no major disabilities unrelated to polio that could cause
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weakness or overuse problems (e.g. stroke, amputation, inflammatory arthritis, peripheral
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neuropathy, muscular dystrophy, or congenital malformation), 3) no serious illnesses such as
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heart or lung disease which would make it unsafe for them to exert themselves in a strength test
106
(e.g. severe emphysema, poorly controlled asthma, resting angina, recent heart attack, or recent
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treatment of an uncontrolled heart condition), and 4) no fractures or surgeries within the
108
previous six months.
109
Of the 290 polio survivors initially screened, 194 participated in the study. Thirty-one
110
individuals were excluded because they did not meet the inclusion criteria. The remaining 65
111
individuals did not participate because of personal reasons (transportation problems, job
112
conflicts, illness/death in family, etc.) or simply did not show up for one or more scheduled
113
appointments. Ultimately, 98 men and 96 women were enrolled in the study. All subjects
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provided written informed consent prior to testing.
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Procedure
The following protocol was approved by our Institutional Review Board. A brief clinical
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interview was conducted to review a standardized medical history questionnaire and a polio
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history form in which subjects specified their age at the time of the initial polio infection and
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identified any sites where they were left with residual weakness or paralysis. There were seven
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possible sites given: neck, back, abdomen, left arm, left leg, right arm, and right leg.
122
Each subject also completed a self-administered activity assessment survey, which was
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developed based on a questionnaire designed to measure habitual physical activity.9 The survey
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included specific activities that might predispose to overuse symptoms and were divided into
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household, occupational, and recreational tasks. Under each heading, the tasks were broken
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down into upper limb activities (e.g. reaching, typing, sewing), lower limb activities (e.g.
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standing, walking, climbing stairs) and transfer activities (moving from sit to stand). For each
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activity, the subjects chose one of four levels that gave the best estimate of the frequency with
129
which they performed that activity. Upper limb, lower limb, and transfer activity levels were
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then calculated by summing the frequency scores in each category.
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After the forms were completed, height (cm) and weight (kg) were measured using a
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standard scale. A nurse then performed a symptom assessment, which included a combination of
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palpation and resistance tests of the biceps and supraspinatus. For the biceps palpation test, the
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shoulder was in neutral rotation, the elbow flexed at 90 degrees and the forearm supinated.
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Pressure was applied in the bicipital groove on the anterior shoulder. The arm was positioned in
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a similar way for the biceps resistance test, except the palm was down. The nurse then attempted
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to supinate the forearm while the subject resisted. For the supraspinatus palpation test, the arm
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was relaxed at the side and pressure was then applied on the tendon insertion site, just proximal
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to the greater tuberosity of the humerus. Finally, for the supraspinatus resistance (impingement)
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test, the arm was held straight out at the side with the thumb pointing towards the floor. The
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nurse pushed on the arm above the elbow while the subject resisted.
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If subjects reported feeling shoulder pain during a symptom test, they were asked if they
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had experienced pain in that area before and if they could identify the estimated date of onset
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(EDO) of the pain. They were also asked to specify activities that caused pain in the same area.
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Pain or tenderness identified as being related to the exam only (i.e. "It only hurts when you push
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there.") was not considered a potential overuse symptom and was not included in any of the
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analyses.
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A manual strength examination was then performed by a physical therapist using a hand-
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held dynamometer (Empi Microfet2, St. Paul, MN). The physical therapist was masked from the
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results of the symptom assessment to prevent any potential bias. The bilateral hip extensor and
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knee extensor muscle groups were tested in gravity-eliminated postures. Bilateral shoulder
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flexion and abduction strength was also measured to account for the possibility that shoulder
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symptoms might be related to shoulder rather than leg weakness. The postures, placement of the
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dynamometer, and stabilization points were standardized (Table 1), along with the verbal
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encouragement used during the testing.
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For each strength test, the subject pushed against the padded dynamometer force plate,
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which the physical therapist held stationary. The peak force was measured in pounds, and the
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range of the dynamometer was 0 to 100 lbs. Two measurements of peak force were taken for
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each muscle group. Additional measurements were taken only if the first two varied by more
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than 10% or by more than 1 lb. for strengths less than 10 lbs. The maximum number of
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"
Insert Table 1 about here.
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—
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measurements for a single muscle group was four to prevent fatigue. If a subject reported pain
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during testing, those trials were considered invalid. For each muscle group, the average of the
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valid trials was used for analysis. However, any muscle groups that did not have two trials that
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met the 10% or lib. criteria after four attempts were not included in any analyses.
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—
In order for individuals to use their arms effectively to help push themselves out of a
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chair, they must have gravity-resistant strength in their elbow extensor muscles. Therefore, once
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the dynamometer testing was completed, the physical therapist performed manual muscle testing
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(MMT) on both elbow extensors using a standardized protocol as described by Kendall, and the
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Lovett grading system.10'11 If the strength was equal to or greater than grade 3, it was specified
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using a plus (+) or a minus (-) sign to designate intermediary levels. If the strength was less than
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a grade 3, a muscle grade of <3 was recorded. Only subjects who had a minimum of grade 3
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strength in both elbow extensors were included in the symptom and strength analyses
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Reliability
Two nurses and three physical therapists were involved in data collection for this study.
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Therefore, it was necessary to get a measure of inter-rater reliability for both the symptom and
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strength assessments.
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Sixteen polio survivors were tested to determine symptom interrater reliability. Nurse #1
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performed the initial assessment for 10 of the subjects and Nurse #2 performed the initial
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assessment for the remaining 6 subjects. A period of one to five days separated the two
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assessments for each subject. All assessments were done at the same time of day.. For
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symptom reliability, p0 or the proportion of observed agreement was calculated by taking the
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number of assessments when both nurses agreed divided by the total number of assessments for
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each of the four symptom tests. All values for p0 were above 93% except for the supraspinatus
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(impingement) test, which was 87%.
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To determine the interrater reliability of the strength measurements, six subjects (2 polio
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survivors and 4 individuals with no history of polio) had their hip extensor, knee extensor,
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shoulder flexion, and shoulder abduction strength tested bilaterally by each of the three physical
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therapists. For each subject, all strength assessments were performed at the same time of day
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within a one month period. Intraclass correlation coefficients (ICC[3,1]12) were used as indices
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of reliability for the strength measurements. All ICC values were above 0.910 except hip
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extension on the dominant side, which was 0.787
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Statistical Analysis
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Data were analyzed using the SYSTAT7 software package. Subjects were classified
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based on whether they had a positive or negative response to each symptom test. In order to
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determine whether certain symptom tests were linked in their occurrence either by structure
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(biceps vs. supraspinatus) or type of test (palpation vs. resistance test), a correspondence analysis
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was performed. The results revealed two distinct clusters that were arbitrarily identified as
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Cluster 1 and Cluster 2. Subjects were then reclassified based on whether or not they had any
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Cluster 1 or Cluster 2 symptoms.
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Biomechanically, there was no reason to believe that the symmetric/assymmetric use of
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the lower extremities was relevant to the production of shoulder symptoms. The knee extensors
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work together to help lift a person off a chair, and the hip extensors work together to help the
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body straighten to a standing position. Therefore, we felt it was appropriate to consider
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combinations of the strengths of similar types of muscles in our analyses, including KNEES (the
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combined strength of both knee extensors), HIPS (the combined strength of both hip extensors),
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and ALL (the combined strength of both knee extensors and both hip extensors).
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In order to determine the nature of the relationship between symptom status and the
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various independent variables (age, time since polio, weight, activity scores and the various
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strength measures), we converted the independent variables to quintiles (i.e. sorted each from
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smallest to largest and separated them into five bins with approximately the same number of
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subjects in each bin). The proportion of subjects in each quintile with either Cluster 1 or Cluster
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2 symptoms was then calculated. Plots of the proportion of subj ects in each symptom cluster
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against the various independent variables (in quintiles) revealed neither a linear pattern nor a
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good fit to a polynomial equation. Therefore, the quintiles were treated as categorical variables
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(1 -5). The only exception was weight. In the plot of the proportion of subj ects with Cluster 1
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symptoms versus weight, we observed an increasing pattern. Therefore, this variable was
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treated as quantitative instead of categorical in the analyses for this symptom cluster. A Chi-
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square analysis was used to evaluate the effect of gender.
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Because of the relatively large number of potential predictor variables, univariate logistic
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regression was performed to eliminate some terms prior to doing a multivariate stepwise logistic
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analysis. A cutoff value of 0.15 was used. In the multivariate analysis, the p-values were
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calculated relative to the highest level or quintile 5 for each independent variable. Odds ratios
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were calculated as a measure of the difference in the proportion of shoulder symptoms between
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quintile 5 and the other quintiles.
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RESULTS
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Subject Characteristics
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The range in age for the study population was 32 to 81 years (mean age: 57 ± 10 yr.).
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The median age at onset of polio was 5 years, and the median number of years since polio was
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48, ranging from 29 to 80 years. As expected, the most common sites for residual weakness
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were the legs (left (57%) and right (55%)). All of the remaining sites had values below 25%.
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Approximately 7% of the subjects stated that they had no residual weakness or paralysis.
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A total of 15 (8%) of the subjects enrolled in the study did not meet the minimum
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requirements for elbow extensor strength (grade 3 or better in both arms). Therefore, their data
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were excluded from the strength and symptom analyses.
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Shoulder Symptoms
Overall, 90 (46%) of the subjects had one or more shoulder symptoms. The
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correspondence analysis showed that there were two distinct symptom clusters. Cluster 1
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consisted of the four palpation tests (left and right biceps palpation and left and right
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supraspinatus palpation). Cluster 2 consisted of the four resistance tests (left and right
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supraspinatus (impingement) tests and left and right biceps tests). Replication of the
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correspondence analysis separately for each gender gave similar results. In both cases, the
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palpation-provoked symptoms formed one cluster and the resistance-provoked symptoms formed
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another.
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There was no significant association between symptom clusters (Chi-square value =
0.060,1 d.f, p = 0.806). Overall, 30 (17%) subjects had palpation-provoked symptoms only, 43
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(24%) subjects had resistance-provoked symptoms only, and 17 (9%) subjects had both types of
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symptoms.
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Palpation Symptom Analysis
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There was a significant association between gender and the presence of palpation
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symptoms (Chi-square value = 15.552,1 d.f, p-value < 0.001). A total of 38 (42%) females had
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palpation symptoms compared to only 9 (10%) males. Because of the relatively low number of
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males with these symptoms, the remaining analyses were performed with females only.
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The results of the univariate logistic regression analysis with presence or absence of
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palpation symptoms as the dependent variable, showed that weight, age, shoulder flexion
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strength, upper limb activity score, KNEES and ALL had p-values below the 0.15 cutoff. When
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these variables were put into a stepwise multivariate logistic regression analysis, the results
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showed that KNEES and weight were the best predictors of the presence of palpation symptoms
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among females. The p-values and odds ratios for the model are listed in Table 2.
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A plot of the proportion of females with palpation symptoms versus KNEES (in
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quintiles) showed evidence of a threshold effect (Figure 1). The proportion of females with
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palpation symptoms was significantly higher when bilateral knee extensor strength was less than
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79 lb. than when it was greater than 79 lb. A plot of the proportion of females with palpation
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symptoms versus weight (in quintiles) revealed that as weight increased, the proportion of
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females with shoulder symptoms also increased (Figure 2).
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Insert Table 2 about here.
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Insert Figure 1 about here.
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Insert Figure 2 about here.
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Resistance Symptom Analysis
A Chi-square analysis showed no significant association between gender and presence of
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resistance symptoms (Chi-square value = 0.025, p - 0.999), with an approximately equal
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proportion of symptomatic subjects for each gender (males: 33% and females: 34%). Therefore,
287
we initially performed the logistic analyses with both genders combined.
288
The results of the univariate analysis, with presence or absence of resistance symptoms as
289
the dependent variable, showed that HIPS, KNEES, ALL, and age all had p-values that were less
290
than the cutoff level of 0.15. The results of the stepwise multivariate analysis showed that the
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model containing ALL and age best predicted the presence of resistance symptoms. The p-
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values and odds ratios for the model are summarized in Table 3.
293
A plot of the proportion of subjects with resistance symptoms versus ALL (in quintiles)
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showed that the highest proportion of symptomatic subjects was found in the mid-range for
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overall leg extensor strength (Figure 3). The plot of the proportion of subjects with resistance
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Insert Table 3 about here.
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symptoms versus age (in quintiles) showed that subjects between the ages of 50 and 54 years,
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had the highest proportion of symptoms (Figure 4).
30i
Because of concern that gender was possibly confounding the results, the analysis was
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repeated on each gender separately. The results of the univariate analysis for males showed that
303
KNEES and age were the only predictors with p-values less than 0.15. The stepwise multivariate
304
analysis resulted in a model containing both variables. Plots of the proportion of males with
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resistance symptoms revealed that the highest proportion of symptomatic males were in the mid-
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range for both bilateral knee extensor strength and age. For females, the results of the univariate
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analysis showed that HIPS, ALL, and age had p-values less than 0.15. The stepwise multivariate
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analysis produced a model containing HIPS and age. The highest proportion of symptomatic
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females was on the low end for both bilateral hip extensor strength and age.
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The odds ratios, sensitivity, and specificity values for the KNEES model and the HIPS
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model for both genders were compared (Table 4). For males, the KNEES model appeared to be
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the best predictor, with larger, more significant odds ratios and a higher sensitivity value model
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than the HIPS model. However, the HIPS model for males had a higher value for specificity
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than the KNEES model. For females, the odds ratios for both the knee and hip models show
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similar patterns, and the sensitivity and specificity values for both models are comparable.
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—
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Insert Figure 3 about here.
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Insert Figure 4 about here.
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_____
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Insert Table 4 about here.
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DISCUSSION
The purpose of this study was to determine if there was a systematic relationship between
327
leg extensor weakness and the presence of pain potentially attributable to shoulder overuse. The
328
results showed that the shoulder symptom tests could be divided into two distinct clusters based
329
on the type of testing used for assessment. The results of the multivariate analyses appear to
330
support the theory that these are two different symptom complexes.
331
Palpation-provoked symptoms were more common among females, as are many overuse
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injuries.13,14 This may be due to differences in pain perception and report. Previous studies have
333
suggested men have a higher pain tolerance than women, especially in tests involving pressure
334
pain.15,16'17 These differences in pain sensitivity have been attributed to a variety of factors
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including differences in body size and skin thickness, sex-role expectations, and hormones. This
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may explain why we did not see a significant gender effect for resistance symptoms, which were
337
assessed with an active motion test as opposed to someone applying pressure to a particular area.
338
In order to determine if gender differences might simply be related to greater stoicism among
339
men, we assessed the severity ratings for the resistance symptoms and found no significant
340
differences (i.e.women did not rate their pain intensity higher than men).
341
Palpation symptoms among women were strongly related to knee extensor strength and
342
weight. The most likely explanation is that weak knee extensors cause increased demand on the
343
arms during tasks such as getting up from a chair or using an assistive device for ambulation.
344
Increased weight will also result in an increased demand on the arms during similar tasks.
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345
Unfortunately, we did not have sufficient power to allow us to distinguish a threshold model
346
from the predicted curvilinear model. From the graph of the proportion of females with
347
palpation-provoked symptoms versus quintiles of knee extensor strength, it did appear that the
348
proportion of symptomatic females was highest in the mid-range for strength. However, it was
349
not possible to determine whether females with moderate weakness were truly at higher risk for
350
shoulder symptoms than profoundly weak subjects or whether this peak was simply due to
351
random error.
352
In terms of predicting resistance symptoms, we were not able to draw any definitive
353
conclusions. While it does appear that some aspect of lower extremity strength is a significant
354
predictor for resistance symptoms for both genders, the results were variable between KNEES,
355
HIPS and ALL, depending on which genders were included in the model. The results for males
356
suggested that knee extensor strength is more important. However, for females the results were
357
not as clear and there remains some doubt as to whether hip extensor, knee extensor strength, or
358
some combination of both is the best predictor for females. Because of the high correlations
359
between strength variables, a larger study is needed to determine which aspect of lower extremity
360
strength is most important when predicting resistance symptoms and whether there are actually
361
any gender-related differences.
362
Shoulder abduction strength was not found to be a significant predictor of shoulder
363
symptoms in this population. Shoulder flexion strength met the cutoff criterion in the univariate
364
analysis for palpation symptoms among females (p-value = 0.150), but was not selected in the
365
stepwise multivariate analysis. Previous research on other populations has shown a relationship
366
between weak shoulder muscles and shoulder symptoms in able-bodied adults (abductors and
367
external rotators)18 and in wheelchair athletes (adductors and internal rotators).19,20 It is possible
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16
368
that other shoulder strength measures such as adductor or internal rotator strength, which were
369
not measured in this study, are related to shoulder symptoms in this population. However,
370
despite this, the fact that knee extensor strength was a good predictor of shoulder symptoms
371
provides support for our hypothesis that lower extremity weakness plays an important role in the
372
production of shoulder symptoms in this population.
373
Age was an important factor for predicting resistance symptoms. We had predicted that
374
duration of time since polio would be more important than chronological age in this population,
375
but duration was not significant even at the univariate level. We had also predicted that
376
symptoms would increase as age increased. However, the results showed that the proportion
377
symptomatic subjects was highest among the younger females and the middle-age males in our
378
study population. We speculate that these age levels may be most closely associated with the
379
activity levels that provoke the symptoms.
380
In able-bodied populations, repetitive manual work is a known risk factor for shoulder
381
symptoms.21'22 A previous study involving 32 polio survivors reported that the experience of
382
pain was related to level of physical activity.5
383
activity level or transfer activity level would be an important factor in predicting the presence of
384
shoulder symptoms. However, none of the activity levels were significant at the univariate level
385
for resistance symptoms and only upper limb activity level was significant at the univariate level
386
for palpation symptoms (p-value = 0.033). One possible explanation is that our activity
387
questionnaire provided us with only a gross measure of upper and lower limb activity. In order
388
to cover individuals with a wide range of strengths and activity levels, we were forced to make
389
our questions as broad as possible. If we had limited our study to individuals with significant
390
lower extremity weakness and concentrated more closely on activities performed by people at
Footline: Leg Weakness and Shoulder Overuse
In this study, we expected that lower limb
17
391
this strength level, we expect that we would have found a stronger association between activity
392
level and shoulder symptoms.
393
Another limitation of this study was that we did not have the power to test interactions
394
between independent variables due to the relatively low percentage of subjects with each
395
symptom cluster. More data are needed in order to capture the complicated synergisms that may
396
exist between variables. For example, we would expect that there would be an interaction
397
between strength and weight. Previous studies have documented that the amount of muscle
398
strength required to perform daily activities increases as weight increases.23'24'25 Weight was an
399
important predictor for palpation symptoms along with overall knee extensor strength. We
400
attempted to capture the interaction between knee strength and weight by calculating the ratio
401
between the two variables (knee extensor strength divided by weight). However, our analysis
402
showed that this ratio did not predict the presence of palpation-provoked symptoms as well as the
403
model with weight and KNEES.
404
Future studies are needed in this area involving larger samples to better characterize the
405
shapes of the distributions of symptom risk. Research involving other populations with varying
406
levels of lower extremity weakness is also needed to determine if these results are generalizable
407
to other groups. For example, the elderly are at high risk for lower extremity weakness due to a
408
reduction in activity level and the decline in muscle strength associated with normal aging. In a
409
sample of 58 subjects with no history of any neuromuscular disorders, aged 60 to 88 years, we
410
found that 39% had bilateral knee extensor strength that was less than 79 lb. (unpublished data).
411
According to our model, these people may be at high risk for development of shoulder overuse
412
symptoms.
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413
Biomechanical studies of the compensation patterns used by people with lower extremity
414
weakness are also needed, both to identify the specific activity patterns and to determine whether
415
there are actual gender differences. Finally, there is a need for studies which examine the
416
effectiveness of therapies designed to either reduce the stress on the shoulders or increase the
417
strength of the lower extremities as a way of preventing or reducing overuse symptoms in the
418
shoulder.
419
420
421
CONCLUSIONS
The results of the present study indicate that there is a relationship between lower
422
extremity weakness and shoulder symptoms. In this sample of polio survivors, knee extensor
423
strength was identified as an important predictor of shoulder symptoms, with individuals with
424
moderate weakness at highest risk. Body weight and age were also relevant factors. These
425
results have important implications for people with significant levels of lower extremity
426
weakness, who tend to increase their reliance on the upper extremities for mobility and activities
427
of daily living. For these people, shoulder overuse problems can have a significant effect on
428
quality of life. Additional research is needed to increase the awareness of the prevalence and
429
impact of upper extremity overuse disorders in people with lower extremity weakness.
430
431
Acknowledgments: The authors would like to thank Roberta Costello, RN, Jeannine Jacobs,
432
RN, Julie Nagorsky, PT, Christina Palmer, PTA, and Steve Sepel, PT for their assistance with
433
data collection. We would also like to thank Yvonne Randolph for her help with recruiting and
434
scheduling subjects. Finally, we gratefully acknowledge the time and effort of our research
435
subjects without whom this research would not have been completed.
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19
436
REFERENCES
437
1. Kibler WB, Chandler TJ, Stracener ES. Musculoskeletal adaptations and injuries due to
438
439
440
441
442
443
overtraining. Exerc Sports Sei Rev 1992; 20: 99-126.
2. Salazar-Grueso EF, Siegel I, Roos RP. The post-polio syndrome: evaluation and treatment.
Comprehensive Therapy 1990; 16(2): 24-30.
3. Perry J, Barnes G, GronleyJ. The postpolio syndrome. Clinical Orthopedics and Related
Research, 233: 145-161,1988.
4. BodianD. Poliomyelitis: pathologic anatomy. In: Poliomyelitis: Papers and Discussions
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Presented at the First International Poliomyelitis Conference. Philadelphia, PA: J.B.
445
Lippincott Company; 1949.
446
447
448
5.. Willen C, Grimby G. Pain, physical activity, and disability in individuals with late effects of
polio. Arch Phys Med Rehabil 1998; 79: 915-919.
6. Perry J, Mulroy SJ, Renwick SE. The relationship of lower extremity strength and gait
449
parameters in patients with post-polio syndrome. Arch Phys Med Rehabil 1993; 74: 165-9.
450
7. Gellman J, Sie I, Waters RL. Late complications of the weight-bearing upper extremity in the
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452
453
454
455
456
457
paraplegic patient. Clin Orthop 1988 Aug; 233: 132-5.
8. Burnham RS, May L, Nelson E, Steadward R, Reid DC. Shoulder pain in wheelchair
athletes: the role of muscle imbalance. Am J Sports Med 1993; 21: 238-42.
9. Baecke JAH, Burema J, Frijters JER. A short questionnaire for the measurement of habitual
physical activity in epidemiological studies. Amer J Clin Nutrition 1982; 26: 936-942.
10. Kendall HO, Kendall FP, Wadsworth GE. Muscles, Testing and Function, Ed 2. Baltimore:
Williams & Wilkins, 1971.
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20
458
459
460
461
462
11. Lovett RW, Martin EG. A method of testing muscular strength in infantile paralysis. JAMA
1915; 65: 1512.
12. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psych Bull
1979; 86(2): 420-428.
13. Hart DA, Archambault JM, Kydd A, Reno C, Frank CB, Herzog W. Gneder and neurogenic
463
variables in tendon biology and repetitive motion disorders. Clin Orthop 1998; 351: 44-56.
464
14. McKeag DB. Overuse injuries: The concept in 1992. Primary Care 1991; 18(4): 851-865.
465
15. Robin 0, Vinard H, Vernet-Maury E, Saumet JL. Influence of sex and anxiety on pain
466
467
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threshold and tolerance. Funct Neurol 1987; 2: 173-179.
16. Unruh AM. Review article: Gender variations in clinical pain experience. Pain 1977; 65:
123-167.
469
17. Weisenberg M. Pain and pain control. Psychol Bull 1977; 84: 1008-1044.
470
18. Hawkins R, Kennedy J. Impingement syndrome in athletes. Am J Sports Med 1980; 8: 151-
471
472
473
474
158.
19. Burnham RS, May L, Nelson E, Steadward R, Reid DC. Shoulder pain in wheelchair
athletes: The role of muscle imbalance. Am J Sport Med 1993; 21: 238-242.
20. Miyahara M, Sleivert GG, Gerrard DF. The relationship of strength and muscle balance to
475
shoulder pain and impingement syndrome in elite quadriplegic wheelchair rugby players. Int
476
J Sports Med 1998; 19: 210-214.
477
478
479
480
21. Putz-Anderson V. Cumulative trauma disorders: a manual for musculoskeletal diseases of
the upper limbs. Philadelphia: Taylor & Francis, 1988.
22. Fulcher SM, Kiefnaber TR, Stern PJ. Upper-extremity tendinitis and overuse syndromes in
the athlete. Clin Sports Med 1998; 17(3): 433-448.
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21
481
482
483
484
485
486
23. Hyatt RH, Whitelaw MN, Bhat A, Scott S, Maxwell JD. Association of muscle strength with
functional status of elderly people. Age Ageing 1990; 19: 330-336.
24. Konczak J, Meeuwsen HJ, Cress ME. Changing affordances in stair climbing: the perception
of maximal climbability in young and older adults. J Exp Psych 1992; 18: 691-697.
25. Büchner DM, DeLateur BJ. The importance of skeletal muscle strength to physical function
in older adults. Ann Behav Med 1991; 13: 91-98.
487
488
489
490
491
492
493
494
495
496
497
498
499
500
501
502
503
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22
504
LEGENDS
505
Figure 1 illustrates the relationship between knee extensor strength and the proportion of females
506
with Cluster 1 (palpation) symptoms. Quintiles of strength among females are shown along the
507
X axis, arrayed from weakest to strongest. The proportion of women with palpation-provoked
508
symptoms in each quintile is shown on the Y axis.
509
510
Figure 2 depicts the relationship between the proportion of females with Cluster 1 (palpation)
511
symptoms and weight. Quintiles of weight, from lightest to heaviest, are shown on the X axis.
512
The bars represent the proportion of women with Cluster 1 (palpation) symptoms in each
513
quintile.
514
515
Figure 3 illustrates the relationship between overall leg extensor strength (ALL) and Cluster 2
516
(resistance) symptoms. The quintiles of strength are arrayed from weakest to strongest along the
517
X axis, and the proportion of subjects with resistance-induced symptoms in each quintile is
518
shown on the Y axis.
519
520
Figure 4 illustrates the relationship between age and Cluster 2 (resistance) symptoms. The
521
quintiles of age are ordered from youngest to oldest along the X axis. The bars represent the
522
proportion of subjects in each quintile with resistance-induced symptoms.
Footline: Leg Weakness and Shoulder Overuse
23
#»
~0'
K\'
^J
n0'
#-J
**>'
^
^
(r,'
Bilateral Knee Extensor Strength (lb)
Weight (kg)
a. 0.0
&'
&'
N#'
Bilateral Leg Extensor Strength (lb)
&'
Age (yr)
Table 1. Symptom Evaluation Protocol
Procedure
Test
Arm Position
Biceps
Shoulder in neutral rotation;
Pressure applied in bicipital
palpation
elbow flexed 90°; forearm
groove on anterior shoulder
supinated
Supraspinatus
Arm relaxing at side;
Pressure applied on tendon
insertion site just proximal
palpation
to greater tuberosity of humerus
Supraspinatus
Arm straight out at side
Examiner pushes on arm above
(impingement)
and internally rotated with
elbow while subject resists
test
thumb pointing towards floor
Biceps test
Shoulder in neutral; elbow
Examiner attempts to supinate
flexed 90°; palm down
forearm while subject resists
Footline: Leg Weakness and Shoulder Overuse
Table 2. Prediction of Shoulder Symptoms Provoked by Palpation
Confidence Interval
Odds Ratio
Upper
Lower
0.000
2.346
3.668
1.500
Knees -1
0.014
13.454
107.589
1.683
Knees - 2
0.020
11.412
88.756
1.467
Knees - 3
0.006
18.526
146.600
2.341
Knees - 4
0.055
6.885
49.428
0.959
Variable*
p-value
Constant
0.000
Weight
*.variables are in quintiles
Footline: Leg Weakness and Shoulder Overuse
Table 3. Prediction of Shoulder Symptoms Provoked by Resistance Tests
Confidence Interval
Odds Ratio
Upper
Lower
0.052
5.833
34.436
0.988
All-2
0.376
2.308
14.717
0.362
All-3
0.044
5.250
30.621
0.900
All-4
0.065
6.000
34.317
1.049
Age-1
0.442
1.634
5.709
0.467
Age-2
0.036
3.916
13.988
1.096
Age-3
0.985
1.012
3.787
0.271
Age-4
0.185
2.337
8.215
0.665
Variable*
p-value
Constant
0.001
All- 1
* variables are in quintiles
Footline: Leg Weakness and Shoulder Overuse
Table 4. Comparison of Regression Models
Model: KNEES and AGE
Males
Variable*
Model: HIPS and AGE
Males
Females
Odds ratio Odds ratio
Females
Variable*
Odds ratio
Odds ratio
KNEES-1
7.269
5.549
fflPS-1
3.995
10.032*
KNEES-2
3.952
2.235
HIPS-2
2.798
2.860
KNEES-3
22.218*
4.838
HIPS-3
3.819
5.793
KNEES-4
2.095
4.870
fflPS-4
1.446
6.406*
AGE-1
2.154
1.567
AGE-1
0.855
2.845
AGE-2
16.396*
3.399
AGE-2
3.979
3.641
AGE-3
11.759*
0.310
AGE-3
4.050*
0.395
AGE-4
3.732
1.215
AGE-4
1.245
1.863
Sensitivity
0.758
0.449
Sensitivity
0.435
0.441
Specificity
0.507
0.693
Specificity
0.702
0.725
Note: The models which resulted from the stepwise multivariate analysis are in bold.
* - variables are in quintiles
t-p<0.05
*-p<0.01
Footline: Leg Weakness and Shoulder Overuse
TABLE 1. SUMMARY OF POST-POLIO RESEARCH
Authors
Length of Study
Population
Muscle(s)
Results
Dalakas et al.(1986)'
27 polio survivors*
(symptomatic)
ave. of8.2yr.
(range 4.5 - 20 yr.)
overall body
score
annual decline
of 1% in mean
score
Munsat, Andres, and
Thibideau (1987)5
6 polio survivors
(symptomatic)
400 to 2100 days
unknown
no significant
change in strength
Agre and
Rodriquez(1990)6
23 polio survivors*
12 controls
2yr.
biceps, hamstring
quadriceps
no significant change
in any variables for
either group
Agre and
Rodriquez (1991)7
44 polio survivors*
38 controls
lyr.
quadriceps (affected
side only11)
no significant change
in any measures for
either group
Muninetal. (1991)9
7 polio survivors*
(symptomatic)
3yr.
quadriceps
29% increase on
affected side, 14% increase
on the nonaffected side
Grimby, Hedberg, and
Henning (1994)2
20 polio survivors*
(12 unstable and
8 stable)
4-5 yr.
quadriceps and
hamstring (affected
side only11)
significant decrease
in all measures for
unstable group; only
for knee flexion in
stable group
Agreetal(1995)3
78 polio survivors*
4yr.
quadriceps and
hamstring (affected
side only^)
significant decrease
in quadriceps
strength only
Grimby, Kvist, and
Grangard(1996)4
18 polio survivors*
4yr.
quadriceps,
hamstrings in
26 legs
total thigh muscle
strength decreased
7.8%+ 2.9%
ave. of 2.1 yr.
(range 199 to
1070 days)
Shld. abductors and
adductors; Elbow
flexors and extensors;
Wrist flexors and
extensors; Hip
abductors, adductors,
and flexors; Knee
flexors and extensors;
Ankle dorsiflexors
and plantarflexors
significant increase in
strength in 10 out of
22 muscles for
symptomatic group;
significant decrease in
1 out of 22 muscles for
asymptomatic group
7 years
quadriceps (affected
side only11)
no significant
difference in rate of
strength loss between
groups
Ivanyietal. (1996)'
Rodriquez, Agre,
and Franke (1997)8
56 polio survivors*
(43 symptomatic
and 13 asymptomatic)
23 polio survivors*
(11 unstable and
12 stable)
14 controls*
* - all subjects were less than 65 years old at initial visit
- if both legs affected, stronger one was tested
11
22
Footline: Strength in Polio Survivors
Table 2. Strength Testing Protocol
Muscle Group
Body Position
Position of Limb
HHD Placement
Stabilization Point
Just proximal to ulnar
styloid
Contralateral shoulder
Shld. Ext. Rotation
Sitting
Shoulder at neutral;
elbow flexed 90°
Shld. Abduction
Supine
Shoulder abducted 90° Midshaft of humerus
Anterior aspect of
shoulder
Shld. Flexion
Sidelying
Shoulder flexed 90
elbow extended
Midshaft of humerus
Anterior aspect of
shoulder
Shld Extension
Sidelying
Shoulder at neutral;
elbow flexed 90°
Proximal to olecranon
Anterior aspect of
shoulder
Elbow Extension
Sidelying
Shoulder at neutral;
elbow flexed 90°
Proximal to ulnar styloid; Shoulder
dorsal surface of forearm
Elbow Flexion
Sidelying
Shoulder at neutral;
elbow flexed 90°
Palmar surface of forearm; Shoulder
proximal to wrist
Wrist Flexion
Sitting
Shoulder at neutral;
elbow flexed 90°
Dorsal aspect of hand
Forearm
Wrist Extension
Sitting
Shoulder at neutral;
elbow flexed 90°
Palmar aspect of hand
Forearm
Hip Abduction
Supine
Hip abducted to 45°;
with contralateral hip
neutral
Proximal to superior pole Hip
of patella on lateral aspect
of thigh
Hip Flexion
Sidelying*
Hip flexed to 30°;
knee flexed 60°
Proximal to superior side
of patella
Pelvis
Hip Extension
Sidelying*
Hip neutral; knee
extended
Proximal to popliteal
crease
Pelvis
Knee Flexion
Sidelying*
Hip flexed 10°; knee
flexed 30°
Proximal to maleoli on
posterior aspect of calf
Anterior aspect of
femur
Knee Extension
Sidelying*
Knee flexed 45°
Proximal to malleoli on
anterior aspect of tibia
Femur
Metatarsals
Tibia
Ankle D. Flexion
Supine
Hip, knee, ankle at 0°
Ankle P. Flexion
Supine
Hip, knee, ankle at 0° Metatarsal heads
Tibia
* Leg positioned on raised powder board
Footline: Strength in Polio Survivors
23
Table 3. Characteristics of Subjects in Upper Extremity Group*
Variable
Present age (years)
Age (at onset of acute polio, years)
Height (cm)
Male Subjects
N = 32
Mean (SD)
Female Subjects
N = 39
Mean (SD)
57.84(11.7)
56.31(8.6)
7.15(6.3)
6.41(6.5)
175.40(7.9)
162.19(6.4)
86.77 (18.4)
70.07 (16.8)
Left Shoulder External Rotator
20.23 (9.4)
15-70 (4.6)
Right Shoulder External Rotator
20.96(7.8)
16.14(4.8)
Left Wrist Flexor
23.06 (7.8)
16-50 (4.7)
Right Wrist Flexor
26.67(6.4)
19.10(5.0)
Left Wrist Extensor
26.69(7.0)
17.92(5.2)
Right Wrist Extensor
26.11(6.7)
18.19(5.8)
Left Shoulder Abductor
30.37(13.1)
19.26(6.2)
Right Shoulder Abductor
29.39(13.3)
18.83(6.6)
Left Shoulder Flexor
34.27(14.3)
21.89(5.5)
Right Shoulder Flexor
34.13(12.0)
21.66(6.8)
Left Shoulder Extensor
36.38(13.3)
23.24(6.0)
Right Shoulder Extensor
34.36(12.2)
21.75(6.7)
Left Elbow Extensor
31.50(15.4)
23.67(6.3)
Right Elbow Extensor
33.95 (8.6)
23.09 (6.8)
Left Elbow Flexor
44.19(14.5)
28.53(7.5)
Right Elbow Flexor
44.55(12.4)
29.70(9.3)
Weight (kg)
Strength (at initial visit lb)
* Reasons for excluding subjects from upper extremity group: 26 subjects had pain during testing, 17^cts were
Sria
for one
one or
or more
muscle groups
groups,: and 6 subjects had initial strength equal to zero m one or more muscle
missing
data for
more muscle
groups
24
Footline: Strength in Polio Survivors
Table 4. Effect Sizes for Upper Extremity Muscles
Muscle Group
Effect Size
Right Wrist Flexor
1.109
Left Shoulder External Rotator
0.794
Left Elbow Extensor
0.758
Left Shoulder Extensor
0.719
Right Elbow Extensor
0.694
Right Shoulder External Rotator
0.670
Right Shoulder Extensor
0.525
Left Wrist Flexor
0.496
Left Shoulder Abductor
0.455
Right Shoulder Flexor
0.455
Left Wrist Extensor
0.448
Right Elbow Flexor
0.444
Left Elbow Flexor
0.421
Right Shoulder Abduction
0.391
Left Shoulder Flexor
0.310
Right Wrist Extensor
0.222
Footline: Strength in Polio Survivors
25
Table 5. Characteristics of Subjects in Lower Extremity Group*
Male Subjects
N = 30
Mean (SD)
Female Subjects
N = 35
Mean (SD)
57.93 (10.6)
54.80 (7.3)
7.55 (6.2)
5.91 (6.2)
Height (cm)
177.10(1.8)
163.14(6.6)
Weight (kg)
84.17(17.8)
71.10(13.8)
Left Hip Flexor
43.21 (13.8)
29.60(10.3)
Right Hip Flexor
45.07(13.1)
30.82 (10.2)
Left Hip Extensor
36.40(11.7)
26.75 (8.9)
Right Hip Extensor
35.79(11.6)
25.56 (8.4)
Left Hip Abductor
42.00 (13.0)
28.22 (8.6)
Right Hip Abductor
38.57(12.4)
25.13(7.7)
Left Knee Flexor
38.80(16.1)
27.97(11.5)
Right Knee Flexor
36.67 (13.2)
22.51(9.7)
Left Knee Extensor
43.20 (20.7)
29.47(13.1)
Right Knee Extensor
45.09 18.8)
32.01 (15.5)
Left Ankle Dorsiflexor
32.45(15.1)
25.40(10.8)
Right Ankle Dorsiflexor
25.72 (13.6)
21.77(10.6)
Left Ankle Plantarflexor
42.25 (16.8)
35.17(14.7)
Right Ankle Plantarflexor
39.10(19.2)
29.56 (14.2)
Variable
Present age (years)
Age (at onset of acute polio, years)
Strength (at initial visit lb)
* Reasons for excluding subjects from lower extremity group: 12 subjects had pain during testing, 13 subjects were
missing data for one or more muscle groups, and 30 subjects had initial strength equal to zero in one or more muscle
groups.
Footline: Strength in Polio Survivors
26
Table 6. Effect Sizes for Lower Extremity Muscles
Muscle Group
Effect Size
Left Ankle Dorsiflexor
1.050
Right Ankle Dorsiflexor
0.856
Left Knee Flexor
0.682
Left Hip Flexor
0.419
Right Hip Flexor
0.383
Right Knee Flexor
0.218
Right Knee Extensor
0.128
Right Hip Extensor
-0.024
Left Hip Abductor
-0.037
Left Hip Extensor
-0.083
Left Knee Extensor
-0.110
Right Hip Abductor
-0.130
Right Ankle Plantarflexor
-0.296
Left Ankle Plantarflexor
-0.368
Footline: Strength in Polio Survivors
27
£.
Table 7. Comparison of Rate of Deterioration of Strength*
in Young and Old Polio Survivors
Mean (SD)
Muscle Group
Young Group
(40-50 yr.)
N=18
Old Group
(60-70 yr.)
N=17
Mann-Whitney U
p-value
Lower Extremity**
-0.031 (2.9)
-0.999(3.1)
0.317
Left Hip Flexor
-2.314(4.4)
-1.858(3.1)
0.621
Right Hip Flexor
-1.055(5.3)
-2.785 (3.9)
0.249
Left Knee Flexor
-2.507 (2.3)
-1.590(2.4)
0.248
Right Knee Flexor
-0.520 (2.6)
-1.460(4.5)
0.756
Left Ankle Dorsiflexor
-4.337 (3.7)
-4.820 (4.2)
0.644
Right Ankle Dorsiflexor
-2.446 (2.0)
-3.592 (3.2)
0.310
* represented by robust slope calculated based on strength data from three visits
** average slope across all lower extremity muscles