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Absolute and Relative Reliability of Pressure Pain Threshold Assessments in the Shoulder Muscles of Participants With and Without Unilateral Subacromial Impingement Syndrome
Absolute and Relative Reliability of Pressure Pain Threshold Assessments in the Shoulder Muscles of Participants With and Without Unilateral Subacromial Impingement Syndrome Jose Diego Sales do Nascimento, PT, MSc,a Francisco Alburquerque-Sendín, PT, PhD,b,c Lorena Passos Vigolvino, PT, MSc,a Wandemberg Fortunato de Oliveira, PT,a and Catarina de Oliveira Sousa, PT, PhDa ABSTRACT Objective: The purpose of this study was to determine the relative and absolute reliability of the pressure pain threshold (PPT) in the shoulder muscles of participants with and without unilateral subacromial impingement syndrome. Methods: Study of intraday intra- and interrater and interday intrarater reliability. Fifty-two participants symptomatic for unilateral subacromial impingement syndrome were divided into 2 groups (SG1 and SG2) of 26 participants each, and 26 participants asymptomatic for shoulder pain took part in the study. Two raters assessed the PPT in 4 shoulder muscles. Each rater assessed symptomatic (SG1) and asymptomatic participants twice on the same day, and one of the raters on 2 different days (SG2). The intraclass correlation coefficient, standard error of measurement (SEM95% and SEM%), and minimum detectable change (MDC95% and MDC%) were calculated. Results: Relative reliability was good or excellent for all assessments, as well as for both groups and raters (intraclass correlation coefficient: 0.87-0.98). The SEM95% values for intra- and interday intrarater measures were between 0.43 and 1.50 kgf/cm2 and SEM% between 6.76 and 12.86%, whereas MDC95% values ranged from 0.60 to 2.12 kgf/cm2 and MDC% from 9.56 to 18.18%. In interrater measures, SEM95% was between 0.58 and 0.77 kgf/cm2 and SEM% between 10.10% and 13.71%, whereas MDC95% varied from 0.82 to 1.08 kgf/cm2 and MDC% from 14.29% to 19.39%. Conclusion: Relative reliability was good or excellent. This study presents absolute reliability values that could be used as a reference in the clinical use of PPT. (J Manipulative Physiol Ther 2019;xx:1-11) Key Indexing Terms: Pain Measurement; Reproducibility of Results; Subacromial Impingement Syndrome
INTRODUCTION Shoulder pain is one of the most common causes of musculoskeletal pain,1,2 with impingement syndrome being the most frequent clinical condition.3 There is evidence that a
Department of Physical Therapy, Federal University of Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil. b Department of Sociosanitary Sciences, Radiology and Physical Medicine, University of Cordoba, Cordoba, Spain. c Maimonides Biomedical Research Institute of Cordoba (IMIBIC), Cordoba, Spain. Corresponding author: Catarina de Oliveira Sousa, PT, PhD, Departamento de Fisioterapia, Universidade Federal do Rio Grande do Norte, Av. Senador Salgado Filho, 3000, Campus Universitario, Lagoa Nova, Natal, RN, CEP 59.078-970, Brazil. (e-mail: [email protected]). Paper submitted December 17, 2018; in revised form April 24, 2019; accepted April 24, 2019. 0161-4754 © 2019 by National University of Health Sciences. https://doi.org/10.1016/j.jmpt.2019.04.002
participants with unilateral subacromial impingement syndrome (SIS) experience a decline in the pressure pain threshold (PPT),4 defined as a measure of pain sensitivity in response to force applied perpendicularly to the skin,5 suggesting a regional hyperalgesia process triggered by peripheral nociception resulting from tissue injury.4 The PPT has been widely used in clinical practice and studies to evaluate the response to treatment in different areas of the body and clinical conditions.4-10 However, pressure pain sensitivity seems to be different between muscles and not uniformly distributed in a same muscle,6,11 or even within an anatomic area.12 Moreover, errors by raters or participants can cause the measure to vary.13,14 The literature contains a number of PPT reliability studies that have shown good relative reliability for PPT measures, as assessed by the intraclass correlation coefficient (ICC), in clinical conditions such as epicondylalgia,15 knee osteoarthritis,10 cervical pain,6 and back pain.16,17 The
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Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
ICC provides total data variability, but not what would be expected in trial-to-trial noise, which may be more suitable for monitoring clinical conditions. To that end, other analyses must be used to assess systematic changes or sampling errors that can occur owing to the variability of the equipment or method used, in addition to inherent biological variability.18 In this respect, Bland-Altman analysis assesses the systematic error and magnitude of the error that are clinically acceptable.19 In addition, it is essential to know the standard error of measurement (SEM) and the difference in measures where real change is attributable to a procedure or intervention, and not the assessment itself, which can be determined by the minimum detectable change (MDC).14 Both measures are necessary for adequate management of clinical conditions. Knowing relative and absolute reliability and how PPTs are present in different muscles will help the clinical management of SIS and contribute to understanding the peripheral4 and central sensitization9,20 process of the symptomatic participants. However, there is little information on the reliability of PPTs in upper limb muscles.6,12,13,21-24 The aim of the present study was to determine intraday intra- and interrater and interday intrarater reliability of PPT assessment in shoulder muscles, examining participants with symptoms of unilateral SIS and others asymptomatic for shoulder pain, and presenting error variance and MDC in the PPT of these assessments. We hypothesized that relative reliability would be good or excellent in all the assessments in both symptomatic and asymptomatic participants.
METHODS Design The reliability study occurred in 2 phases: the first included intraday intrarater and interrater reliability and the second included interday intrarater reliability. The study, conducted between May 2016 and October 2017, was approved by the Research Ethics Committee of the Federal University of Rio Grande do Norte (Protocol 1.529.040). All participants gave their informed consent after being advised of the objectives, risks, and benefits of the research. The present study followed the Guidelines for Reporting Reliability and Agreement Studies.25
Participants A total of 78 participants took part in the research. Fifty-two participants symptomatic for unilateral SIS were divided into 2 symptomatic groups (SG1 and SG2) with 26 participants in each one, and 26 asymptomatic participants were allocated in the asymptomatic group (AG) for unilateral SIS. The participants from SG1 and AG were
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submitted to intraday intrarater assessment, where raters 1 and 2 evaluated the same participants on the same day. Only SG1 data were analyzed to assess interrater reliability. The SG2 was submitted to interday intrarater evaluation, where a same rater assessed the same participant on 2 different days. The symptomatic participants were recruited through flyers distributed at universities, gyms, and physical therapy and orthopedic clinics in the city and via social media. The symptomatic participants were allocated into SG1 and SG2 groups according to their availability to perform the assessment on 1 or 2 days. Asymptomatic participants were recruited from the student body and teaching staff of the local university through invitations. Table 1 shows sample characterization. The following inclusion criteria were adopted for the symptomatic participants: age between 18 and 60 years and history of unilateral shoulder pain for at least 1 month, regardless of the pain level, in the proximal anterolateral region,26 or C5 or C6 dermatomes,27 as determined by 3 of the following positive tests: Neer,28 Hawkins-Kennedy,29 Jobe,30 painful arc,3 external rotation resistance,31 Gerber, and Speed.32 The tests used to diagnose SIS usually exhibit high specificity or sensitivity, and the combination of these clinical tests is recommended to identify patients with SIS.3 The following exclusion criteria were established: bilateral SIS, adhesive capsulitis, history of symptom onset owing to trauma, multidirectional or anterior instability of the glenohumeral joint based on the inferior sulcus and positive grip tests, upper-extremity numbness and tingling, fibromyalgia or rheumatic disease, previous neck and shoulder surgery, systemic disease, body mass index (BMI) > 28 kg/m2, corticosteroid injection 3 months before evaluation or use of analgesics or muscle relaxants 72 hours before assessment, and depressive symptoms with a Beck Depression Inventory score 13.33,34 Asymptomatic participants did not present any inclusion or exclusion criteria exhibited for the symptomatic group, and they were matched for sex, age (±5 years), and BMI (±2 kg/m2) with symptomatic participants from SG1.
Raters and Training A digital mechanical pressure algometer (Wagner Instruments, Greenwich, Connecticut) was used to assess PPTs. This device consists of a 1-cm2 rubber disc connected to a pressure gauge, which displays values in kgf/cm2. Two raters with no clinical experience in evaluating PPTs participated in the study: a physical therapy student in the final year and a recently graduated physical therapist. Both raters underwent training to assess PPTs, to standardize the force applied in the algometer to reach a rate of 0.50 kgf/s, as previously described.6 To that end, training consisted of applying pressure on a rigid surface for
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Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
Table 1. Demographic Characteristics of All Participants Sex Age (y)
Symptomatic Group 1 (n ¼ 26)
Symptomatic Group 2 (n ¼ 26)
Asymptomatic Group (n ¼ 26)
P value
12 M; 14 F
16 M; 10 F
12 M; 14 F
.44
29 ± 17.50
35.12 ± 9.73
28 ± 17.50
.89
Height (m)
1.67 ± 0.07
1.67 ± 0.08
1.69 ± 0.09
.68
Weight (kg)
67.52 ± 8.93
68.4 ± 11.6
68.54 ± 11.70
.92
BMI (kg/m2)
24.26 ± 2.75
24.42 ± 2.52
23.99 ± 3.18
.92
6.19 ± 3.44
5.80 ± 0.86
3.50 ± 6.25
.11
Duration of symptoms (mo)
20.65 ± 21.88
19.48 ± 20.37
e
.52
Affected side (right/left)
20 D/6 ND
19 D/7 ND
e
.75
BDI (0/21)
Data are shown as frequency (sex, affected side), mean, and standard deviations (other data). BDI, Beck Depression Inventory; BMI, body mass index; D, dominant; F, female; M, male; ND, nondominant.
5 seconds. An application rate of approximately 2.50 ± 0.25 kgf was considered satisfactory.6 Training was coordinated by a physical therapist with 6 years of experience and totaled 5 hours per examiner.
Assessment Procedures The following muscles were assessed: lower trapezius (in the muscle belly, halfway between the midpoint of the medial border of scapula and the spinous process of the twelfth thoracic vertebra),35 upper trapezius (halfway between the C7 spinous process and acromion process), infraspinatus (in the muscle belly below the midpoint of the spine of scapula), and medial deltoid (muscle belly, near the inferolateral insertion).4 These muscles were selected for being related to scapular stabilization and positioning (upper and lower trapezius), belonging to the rotator cuff (infraspinatus), and being the primary motor in raising the arm in the scapular plane (medial deltoid). Only the affected side was assessed in participants with SIS, whereas the dominant side was evaluated in asymptomatic participants. All the points where pressure was applied with the digital algometer were previously marked by the physical therapist. Participants were assessed in the sitting position, with upper extremities relaxed and forearms resting on their thighs. For interrater and intrarater reliability, assessment was divided into 2 steps for both the SG1 and AG. In the initial step, one of the raters evaluated the participants, and after 5 minutes, the other did. Participants rested for 5 minutes between the first and second steps, which occurred similarly to the first. As such, each rater performed the same assessment twice, obtaining interrater and intrarater reliability on the same day. Two measuring circuits were performed for PPT measures, obtaining 1 measure in each circuit for each
muscle. The second circuit started as soon as the first one was completed. The sequence of muscle assessment and raters was conducted randomly using the website www. randomization.com, maintaining the same sequence in all the circuits, to ensure a constant period between the assessments of each muscle. To obtain interday intrarater measures, the SG2 was evaluated as described earlier, except the second step occurred 48 hours after the first, only on the affected side and assessed by only 1 rater (rater 2). Before starting the PPT assessment procedure, the participants were familiarized with the algometer, which consisted of a single evaluation in a muscle remote from those selected for assessment to ensure they understood the process. The pressure applied with the algometer occurred perpendicularly to the muscle fibers, and the following standard instruction was given: “I am going to start applying pressure to your muscle with this instrument. When the pressure becomes uncomfortable, say stop.”6 During measurements, the raters could not see the device’s display screen, and the PPT values were recorded by an experienced physical therapist.
Statistical Analysis The sample size was determined using Tama~no de la Muestra 1.1 software. Very good reliability was adopted (ICC 0.81)36 with variability of 0.2 and a ¼ 0.05,37 and a sample of 25 participants per group was estimated. Descriptive and inferential statistics were obtained using the SPSS statistical package, version 20.0 (IBM SPSS Statistics for Windows, IBM Corp., Armonk, NY). Means and standard deviations (SDs) were calculated for each variable. Sample distribution was assessed by applying the Shapiro-Wilk test. To investigate differences among groups for demographic and clinical data, 1-way analysis of
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variance (age, height, weight, BMI, and Beck Depression Inventory), c2 (sex), and Mann-Whitney U (symptom duration and affected side) tests were used, adopting a significance value of P < .05. For PPTs, the difference between the means of each assessment was calculated using the paired t and Wilcoxon tests for intrarater measures. Measures from the second assessment of each rater were used for interrater comparison. The ICC (ICC2,1) was calculated to estimate the relative reliability of intraday intrarater and interrater and interday intrarater measures.38 The ICC provides an estimate of population variances based on the variability in a particular set of measures.38 The ICC values less than 0.5 are indicative of poor reliability, values between 0.5 and 0.75 indicate moderate reliability, values between 0.75 and 0.9 indicate good reliability, and values greater than 0.90 indicate excellent reliability.38 Absolute reliability was estimated by calculating the SEM and MDC. The SEM indicates the standard error of the mean, and the MDC the value at which real change 14 occurred, in addition to the measurement pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi error. The SEM can be calculated by SD 1 ICC, and MDC by the formula MDC ¼ SEM √2. The SEM and MDC values were multiplied by 1.96 to obtain a 95% CI.6 To indicate the variation in absolute reliability, expressed in SEM percentage, the SEM%, obtained by MEAN 100, and MDC MDC%, by MEAN 100, were calculated,18 where the mean in the equation corresponds to all the data for the 2 test occasions (intrarater and intraday interrater or interday intrarater). Bland-Altman analysis was conducted to identify systematic biases and 95% limits of agreement (LOA) for each muscle19 using a dispersion graph of the differences and the means of assessments. The difference in mean (d) between the raters and the SD was quantified for this difference (SDd) to obtain 95% LOA. Next, d ± 1.96SDd was calculated, indicating the total error (bias and random error). If 0 is other than 95% LOA, there are systematic differences (biases) between the raters.15
RESULTS The demographic characteristics of participants belonging to the 3 groups are presented in Table 1. No intergroup difference was detected for any of the variables.
Journal of Manipulative and Physiological Therapeutics Month 2019
good (0.90), as well as in the AG for both raters and all measures (ICC ¼ 0.91-0.98). Interrater reliability in SG1 was between good and excellent for all measures, with the ICC varying between 0.87 and 0.94. Regarding interday intrarater assessment, reliability was excellent for all the muscles assessed by rater 2, with an ICC between 0.95 and 0.96.
Absolute Reliability Table 3 shows the absolute reliability values. In general, intraday intrarater measures for the SG1 showed SEM95% between 0.43 and 0.75 kgf/cm2 and SEM% between 7.44% and 12.86%, and MDC95% between 0.60 and 1.06 kgf/cm2 and MDC% between 10.52% and 18.18%. For the AG, SEM95% varied from 0.61 to 1.50 kgf/cm2 and SEM% between 6.76% and 11.47%, and MDC95% from 0.87 to 2.12 kgf/cm2 and MDC% between 9.56% and 16.22%. Interrater reliability measures showed SEM95% values ranging from 0.58 to 0.77 kgf/cm2 and SEM% between 10.10% and 13.71%, and MDC95% from 0.82 to 1.08 kgf/ cm2 and MDC% between 14.29% and 19.39%. For interday intrarater measures, SEM95% varied between 0.61 and 0.82 kgf/cm2 and SEM% between 9.82% and 11.09%, and MDC95% from 0.86 to 1.16 kgf/cm2 and MDC% from 13.88% to 15.69%. The highest SEM95% , SEM%, MDC95%, and MDC% values for each assessment are highlighted in Table 3. Table 3 also shows the 95% LOA values for each muscle in intraday intrarater and interrater and interday intrarater assessment. The amplitude variation in intraday intrarater measures ranged from 1.56 to 3.44 kgf/cm2, for SG1 and AG, interrater between 2.32 and 2.86 kgf/cm2, and interday intrarater between 2.36 and 3.47 kgf/cm2. Figure 1 shows the Bland-Altman plots for rater 2 (intraday and interday intrarater assessments) and intraday interrater values, demonstrating that the difference in means is close to 0, with nonsignificant bias. In both intraday and interday intrarater assessments, bias was between -0.05 and 0.13, and interrater measures between 0.17 and 0.59. Outliers were present in more than 1 assessment (upper trapezius and infraspinatus muscles), and interday assessment values of the infraspinatus and medial deltoid muscles were more dispersed, although linear regression indicated no biased behavior in the variables.
DISCUSSION Relative Reliability Table 2 shows relative intraday intrarater and interrater and interday intrarater reliability. Comparisons of PPT measures in each assessment (intraday and interday; intraand interrater) revealed no difference. The intraday assessment reliability of SG1 was excellent for both raters (ICC ¼ 0.93-0.97) for all the muscles, with the exception of upper trapezius for rater 2, which was considered
As hypothesized, our study showed good or excellent reliability indices in intraday intrarater and interrater and interday intrarater assessments, indicating that algometry is a reliable assessment. We also present SEM and MDC values for intraday assessment and after 48 hours for symptomatic and asymptomatic participants, which could be used as reference values to help interpret PPT changes in interventions and clinical research.
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Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
Table 2. Relative Reliability of Pressure Pain Threshold for Intraday Intrarater and Interrater and Interday Intrarater Evaluations Groups
Upper Trapezius
Lower Trapezius
Infraspinatus
Middle Deltoid
ICC
0.95
0.95
0.93
0.96
95% CI
0.90-0.98
0.88-0.97
0.84-0.97
0.92-0.98
Assessment 1 (kgf/cm2)
2.57 ± 0.96
3.84 ± 1.26
3.71 ± 1.48
3.32 ± 1.36
3.70 (1.39)a
3.47 (1.47)a
2.92 (0.95)a
3.75 ± 1.35
3.62 ± 1.41
3.21 ± 1.33
3.55 (1.61)a
3.06 (2.09)a
2.85 (1.68)a
Intraday Intrarater SG1 (N ¼ 26) Rater 1
2.39 (0.67)a Assessment 2 (kgf/cm2)
2.44 ± 0.99 2.33 (0.94)a
P
.10
.40
.80
.25
ICC
0.90
0.96
0.95
0.97
95% CI
0.78-0.95
0.91-0.98
0.90-0.98
0.94-0.98
Assessment 1 (kgf/cm2)
2.30 ± 1.01
3.21 ± 1.25
3.40 ± 1.44
3.10 ± 1.35
2.91 (1.04)a
3.04 (1.41)a
2.80 (1.08)a
3.15 ± 1.23
3.41 ± 1.56
3.03 ± 1.33
3.07 (1.34)a
3.35 (1.37)a
2.80 (1.41)a
Rater 2
e Assessment 2 (kgf/cm2)
2.26 ± 0.87 e
P
.71
.63
.60
.27
ICC
0.95
0.92
0.95
0.91
95% CI
0.90-0.98
0.83-0.96
0.88-0.97
0.81-0.96
Assessment 1 (kgf/cm2)
3.03 ± 1.12
4.45 ± 1.52
4.44 ± 1.53
3.40 ± 1.20
e
4.42 (2.46)
e
4.47 ± 1.80
4.47 ± 1.80
3.29 ± 1.42
e
4.46 (2.75)a
e
AG (N ¼ 26) Rater 1
2.79 (1.54)a Assessment 2 (kgf/cm2)
3.09 ± 1.35 3.14 (2.01)a
P
.78
.87
.68
.44 (continued on next page)
The literature contains a number of PPT reliability studies showing that digital algometer assessment is reliable, exhibiting high ICC indices,1,6,20,22,38,39 as
observed in the present study. In addition to confirming measurement reliability, it is essential to understand its pattern under different conditions, to determine
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Table 2. (continued) Groups
Upper Trapezius
Lower Trapezius
Infraspinatus
Middle Deltoid
ICC
0.98
0.95
0.97
0.96
95% CI
0.95-0.99
0.89-0.97
0.94-0.98
0.91-0.98
Assessment 1 (kgf/cm2)
2.79 ± 1.28
3.86 ± 1.55
3.84 ± 1.88
2.99 ± 1.33
e
3.67 (2.49)a
3.06 ± 1.28
3.98 ± 1.65
3.97 ± 1.98
e
e
3.83 (2.51)a
Rater 2
2.46 (1.70)a Assessment 2 (kgf/cm2)
2.80 ± 1.41 2.44 (1.93)a
P
.87
.41
.51
.51
ICC
0.87
0.89
0.93
0.94
95% CI
0.70-0.94
0.38-0.96
0.85-0.97
0.88-0.97
Intraday Interrater SG1 (N ¼ 26)
P
.59
.09
.58
.47
ICC
0.95
0.95
0.96
0.96
95% CI
0.90-0.98
0.90-0.98
0.92-0.98
0.91-0.98
Assessment 1 (kgf/cm2)
2.90 ± 1.47
3.53 ± 1.58
4.04 ± 2.12
3.28 ± 1.85
e
3.30 (2.55)a
2.43 (1.98)a
3.46 ± 1.57
4.00 ± 2.08
3.25 ± 1.82
e
3.45 (2.03)a
2.72 (1.80)a
Interday Intrarater SG2 (N ¼ 26)
2.30 (1.93)a Assessment 2 (kgf/cm2)
2.77 ± 1.36 2.30 (1.22)a
P
.92
.96
.98
.19
Values expressed as mean and standard deviation and used paired t test unless otherwise indicated. ICC, intraclass correlation coefficient; SG1, symptomatic group 1; SG2, symptomatic group 2. a Values expressed in median and range interquartile and used Wilcoxon test.
measurement variability in each clinical condition. To that end, it is important to verify the error variance between measures (LOA) in addition to the SEM and its MDC. Our LOA values show that amplitude varied from 1.56 kgf/cm2 to 2.94 kgf/cm2 in intraday intrarater (both raters) and interrater assessments, with the infraspinatus exhibiting the highest amplitude in interday assessment (2.36-3.47 kgf/cm2). Thus, although algometry is reproducible for shoulder muscles in participants symptomatic for SIS, our results suggest that clinical outcomes should be interpreted with caution. The variability of PPT measures may be explained by the different rate of pressure increase and reaction time of the
raters when asked to stop applying pressure.15 Additionally, the muscles evaluated in the present study have frequently been related to myofascial pain syndrome in participants with and without SIS,4,8,9 which causes peripheral sensitization provoked by continuous nociceptive afferents from the clinical condition.4 This may lead to more variable pain perception in these participants. Although training tends to minimize this problem, it is difficult to reproduce the same assessment condition because the muscles may resist differently to the applied pressure owing to the difference in tonus between them, and pressure pain sensitivity is likely not uniformly distributed between the muscle belly and tendons of the
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Table 3. Absolute Reliability Indicators of Pressure Pain Threshold for Intraday Intrarater and Interrater and Interday Intrarater Assessments Groups
Upper Trapezius
Lower Trapezius
Infraspinatus
Middle Deltoid
Intraday Intrarater SG1 (N ¼ 26) Rater 1 SEM95% (kgf/cm2)
0.43
0.62
0.75
0.52
SEM%
8.43
8.27
10.23
8.06
MDC95% (kgf/cm2)
0.60
0.88
1.06
0.74
MDC%
11.92
11.70
14.47
11.40
LOA (kgf/cm2)
-0.65 to 0.91 (1.56)
-1.07 to 1.25 (2.32)
-1.38 to 1.56 (2.94)
-0.86 to 1.06 (1.92)
Rater 2 SEM95% (kgf/cm2)
0.58
0.48
0.65
0.45
12.86
7.67
9.79
7.44
0.82
0.68
0.92
0.64
MDC%
18.18
10.85
13.84
10.52
LOA (kgf/cm2)
-1.08 to 1.16 (2.24)
-0.90 to 1.01 (1.91)
-1.24 to 1.22 (2.46)
-0.76 to 0.88 (1.64)
SEM% MDC95% (kgf/cm2)
AG (N ¼ 26) Rater 1 SEM95% (kgf/cm2)
0.85
1.20
0.94
0.70
SEM%
9.38
10.50
9.67
11.47
MDC95% (kgf/cm2)
1.20
1.70
1.32
0.99
MDC%
13.27
14.85
13.67
16.22
LOA (kgf/cm2)
-1.11 to 1.01 (2.12)
-1.74 to 1.70 (3.44)
-1.61 to 1.49 (3.10)
-1.32 to 1.54 (2.86)
Rater 2 SEM95% (kgf/cm2)
0.61
1.02
0.66
1.50
SEM%
6.76
9.20
8.65
8.65
MDC95% (kgf/cm2)
0.87
1.45
0.93
2.12
MDC%
9.56
13.01
12.23
12.23
-1.33 to 1.07 (2.40)
-1.48 to 1.26 (2.74)
-1.08 to 0.96 (2.04)
LOA (kgf/cm2)
-0.74 to 0.72 (1.46)
(continued on next page)
same muscle.11,12 Intraparticipant reliability should also be considered because patient interpretation of discomfort may change, especially in interday assessments. These factors may be important sources for the different
PPT measures and should be considered in clinical assessment. Error and minimum change values can be interpreted using SEM% and MDC%, which provide variability data as
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Table 3. (continued) Groups
Upper Trapezius
Lower Trapezius
Infraspinatus
Middle Deltoid
Intraday Interrater SG1 (N ¼ 26) SEM95%(kgf/cm2)
0.66
0.63
0.77
0.58
13.71
11.62
10.78
10.10
0.93
0.89
1.08
0.82
MDC%
19.39
16.44
15.25
14.29
LOA (kgf/cm2)
-1.04 to 1.40 (2.44)
-0.59 to 1.77 (2.36)
-1.23 to 1.63 (2.86)
-0.99 to 1.33 (2.32)
SEM% MDC95%(kgf/cm2)
Interday Intrarater SG2 (N ¼ 26) SEM95% (kgf/cm2)
0.61
0.68
0.82
0.71
10.71
9.82
10.31
11.09
0.86
0.96
1.16
1.01
MDC%
15.15
13.88
14.57
15.69
LOA (kgf/cm2)
-1.05 to 1.31 (2.36)
-1.23 to 2.24 (3.47)
-1.48 to 1.54 (3.02)
-1.37 to 1.41 (2.78)
SEM% MDC95% (kgf/cm2)
AG, asymptomatic group; LOA, limits of agreement; MDC, minimum detectable change; SEM, standard error of measurement; SG1, symptomatic group 1; SG2, symptomatic group 2.
Fig 1. Bland-Altman plots for rater 2 (intraday and interday intrarater assessments) and intraday interrater values. The dashed line represents the bias and the solid line represents the limits of agreement.
Journal of Manipulative and Physiological Therapeutics Volume xx, Number xx
a function of the absolute value of the variable, expressed in percentage. As such, considering shoulder muscles, the variation of these measures is generally less than 15% in most intraday intrarater assessments, with only 2 exceptions (upper trapezius in SG1, rater 2, and middle deltoid in AG, rater 1), whereas in intraday interrater and interday intrarater assessments, the variation was greater, but still less than 20%. Thus, change must be at least 20% of MDC% to be deemed meaningful. Nevertheless, there is no acceptable agreement regarding these measures, that is, whether these slight differences could significantly affect clinical practice. The highest SEM95%, MDC95%, SEM%, and MDC% values in Table 3 are similar for all the muscles in both symptomatic and asymptomatic participants, but the latter obtained higher values. Moreover, our results show higher values than those of a previous reliability study. We found SEM95% and MDC95% values of 0.53 and 0.82 kgf/cm2, respectively, for the upper trapezius, whereas Walton et al6 reported 0.41 and 0.58 kgf/cm2. These differences may be related to the sources of PPT measurement variability previously mentioned. In summary, the present study presents PPT values for the shoulder muscles that may contribute to clinical practice. However, the results should be interpreted with caution because error intervals and minimum clinical change can vary between examiners and assessments. As such, we underscore the need for each examiner to know their own absolute reliability as a function of the population under study. The present study exhibits a number of limitations, such as not being able to divide the sample according to sex and age group to assess possible differences between men and women and age range. Although some studies have reported that women have a lower PPT40 and that the aging process also provokes this decline,41 there is still no consensus, especially regarding reliability measures.40 Further, the participants were not categorized for pain intensity, which could provide information on the relation between tissue irritability and reliability. Finally, the current study did not allow knowing how the clinical experience of the raters and participants might affect these measures. Studies that bridge these gaps could lead to more adequate use of the PPT.
Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
FUNDING SOURCES
This study provides evidence that the relative reliability of PPT assessment is good or excellent in intraday intrarater and interrater and interday intrarater evaluations in participants symptomatic for unilateral SIS and their asymptomatic counterparts. Moreover, absolute reliability values related to raters (intrarater or interrater), participants’ clinical condition, and sequence of assessments (intraday and interday) may be useful as references when interpreting PPT measurements in participants symptomatic or asymptomatic for SIS.
CONFLICTS
OF INTEREST
The first author received a master scholarship from CAPES e Brazilian Federal Agency for Support and Evaluation of Graduate Education within the Ministry of Education of Brazil during the conduct of the study. No conflicts of interest were reported for this study.
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): J.D.S.N., C.O.S., F.A.S. Design (planned the methods to generate the results): J.D.S.N., C.O.S., F.A.S. Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): J.D.S.N., C.O.S. Data collection/processing (responsible for experiments, patient management, organization, or reporting data): J.D.S.N., W.F.O., L.P.V. Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): J.D.S.N., C.O.S., F.A.S., L.P.V., W.F.O. Literature search (performed the literature search): J.D.S.N., C.O.S. Writing (responsible for writing a substantive part of the manuscript): J.D.S.N., C.O.S., F.A.S. Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): C.O.S., F.A.S.
Practical Applications
CONCLUSION
AND
The relative reliability of PPTs in the shoulder muscles is, overall, excellent for both symptomatic and asymptomatic participants for shoulder pain. The error intervals and MDCs of PPTs of shoulder muscles are provided. Error intervals and MDC values provided can be used to interpret PPT measures in shoulder muscles in interventions and clinical research. The findings should be interpreted with caution, given that error intervals and MDCs could vary depending on the rater and assessments, as well as sex or age of the participants.
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REFERENCES 16. 1. Saracoglu I, Emuk Y, Taspinar F. Does taping in addition to physiotherapy improve the outcomes in subacromial impingement syndrome? A systematic review. Physiother Theory Pract. 2018;34(4):251-263. 2. Sergienko S, Kalichman L. Myofascial origin of shoulder pain: a literature review. J Bodyw Mov Ther. 2015;19(1):91-101. 3. Michener LA, Walsworth MK, Doukas WC, Murphy KP. Reliability and diagnostic accuracy of 5 physical examination tests and combination of tests for subacromial impingement. Arch Phys Med Rehabil. 2009;90(11):1898-1903. 4. Alburquerque-Sendín F, Camargo PR, Vieira A, Salvini TF. Bilateral myofascial trigger points and pressure pain thresholds in the shoulder muscles in patients with unilateral shoulder impingement syndrome. Clin J Pain. 2013;29(6): 478-486. 5. Alburquerque-Sendín F, Madeleine P, Fernandez-de-lasPe~nas C, Camargo P, Salvini T. Spotlight on topographical pressure pain sensitivity maps: a review. J Pain Res. 2018;11: 215-225. 6. Walton DM, Macdermid JC, Nielson W, Teasell RW, Chiasson M, Brown L. Reliability, standard error, and minimum detectable change of clinical pressure pain threshold testing in people with and without acute neck pain. J Orthop Sports Phys Ther. 2011;41(9):644-650. 7. Cunha CO, Pinto-Fiamengui LMS, Castro ACPC, Lauris JRP, Conti PCR. Determination of a pressure pain threshold cut-off value for the diagnosis of temporomandibular joint arthralgia. J Oral Rehabil. 2014;41(5):323-329. 8. Hidalgo-Lozano A, Fernandez-de-las-Pe~nas C, DíazRodríguez L, Gonzalez-Iglesias J, Palacios-Ce~na D, ArroyoMorales M. Changes in pain and pressure pain sensitivity after manual treatment of active trigger points in patients with unilateral shoulder impingement: a case series. J Bodyw Mov Ther. 2011;15(4):399-404. 9. Hidalgo-Lozano A, Fernandez-de-las-Pe~nas C, AlonsoBlanco C, Ge H-Y, Arendt-Nielsen L, Arroyo-Morales M. Muscle trigger points and pressure pain hyperalgesia in the shoulder muscles in patients with unilateral shoulder impingement: a blinded, controlled study. Exp Brain Res. 2010; 202(4):915-925. 10. Srimurugan Pratheep N, Madeleine P, Arendt-Nielsen L. Relative and absolute test-retest reliabilities of pressure pain threshold in patients with knee osteoarthritis. Scand J Pain. 2018;18(2):229-236. 11. Ohrbach R, Gale EN. Pressure pain thresholds in normal muscles: reliability, measurement effects, and topographic differences. Pain. 1989;37(3):257-263. 12. Ribeiro IL, Camargo PR, Alburquerque-Sendín F, Madeleine P, Fernandez-de-las-Pe~nas C, Salvini TF. Topographical pressure pain sensitivity maps of the shoulder region in individuals with subacromial pain syndrome. Man Ther. 2016;21:134-143. 13. Chesterton LS, Sim J, Wright CC, Foster NE. Interrater reliability of algometry in measuring pressure pain thresholds in healthy humans, using multiple raters. Clin J Pain. 2007; 23(9):760-766. 14. Weir JPJ. Quantifying test-retest reliability using the intraclass correlation coefficient and the SEM. J Strength Cond Res. 2005;19(1):231-240. 15. Smidt N, Van der Windt DA, Assendelft WJ, et al. Interobserver reproducibility of the assessment of severity of complaints, grip strength, and pressure pain threshold in
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patients with lateral epicondylitis. Arch Phys Med Rehabil. 2002;83(8):1145-1150. Balaguier R, Madeleine P, Vuillerme N. Intra-session absolute and relative reliability of pressure pain thresholds in the low back region of vine-workers: effect of the number of trials. BMC Musculoskelet Disord. 2016;17(1):350. Balaguier R, Madeleine P, Vuillerme N. Is one trial sufficient to obtain excellent pressure pain threshold reliability in the low back of asymptomatic individuals? A test-retest study. PLoS One. 2016;11(8):e0160866. Lexell JE, Downham DY. How to assess the reliability of measurements in rehabilitation. Am J Phys Med Rehabil. 2005;84(9):719-723. Bland JM, Altman DG. Measuring agreement in method comparison studies. Stat Methods Med Res. 1999;8(2):135-160. Paul TM, Soo Hoo J, Chae J, Wilson RD. Central hypersensitivity in patients with subacromial impingement syndrome. Arch Phys Med Rehabil. 2012;93(12):2206-2209. Bisset LM, Evans K, Tuttle N. Reliability of 2 protocols for assessing pressure pain threshold in healthy young adults. J Manipulative Physiol Ther. 2015;38(4):282-287. Park G, Kim CW, Park SB, Kim MJ, Jang SH. Reliability and usefulness of the pressure pain threshold measurement in patients with myofascial pain. Ann Rehabil Med. 2011;35(3): 412. Vanderweeen L, Oostendorp RA, Vaes P, Duquet W. Pressure algometry in manual therapy. Man Ther. 1996;1(5):258-265. Ylinen J, Nyk€anen M, Kautiainen H, H€akkinen A. Evaluation of repeatability of pressure algometry on the neck muscles for clinical use. Man Ther. 2007;12(2):192-197. Kottner J, Audige L, Brorson S, et al. Guidelines for Reporting Reliability and Agreement Studies (GRRAS) were proposed. Int J Nurs Stud. 2011;48(6):661-671. Lin J, Chen W-H, Chen P-Q, Tsauo J-Y. Alteration in shoulder kinematics and associated muscle activity in people with idiopathic scoliosis. Spine (Phila Pa 1976). 2010;35(11): 1151-1157. Struyf F, Nijs J, Baeyens J-P, Mottram S, Meeusen R. Scapular positioning and movement in unimpaired shoulders, shoulder impingement syndrome, and glenohumeral instability. Scand J Med Sci Sports. 2011;21(3):352-358. Neer CS. Anterior acromioplasty for the chronic impingement syndrome in the shoulder: a preliminary report. J Bone Joint Surg Am. 1972;54(1):41-50. Hung CJ, Jan MH, Lin YF, Wang TQ, Lin JJ. Scapular kinematics and impairment features for classifying patients with subacromial impingement syndrome. Man Ther. 2010; 15(6):547-551. Jobe FW, Jobe CM. Painful athletic injuries of the shoulder. Clin Orthop Relat Res. 1983;173:117-124. Diercks R, Bron C, Dorrestijn O, et al. Guideline for diagnosis and treatment of subacromial pain syndrome. Acta Orthop. 2014;85(3):314-322. Camargo PR, Avila MA, Asso NA, Salvini TF. Muscle performance during isokinetic concentric and eccentric abduction in subjects with subacromial impingement syndrome. Eur J Appl Physiol. 2010;109(3):389-395. Altindag O, Gur A, Altindag A. The relationship between clinical parameters and depression level in patients with myofascial pain syndrome. Pain Med. 2008;9(2):161-165. Furlanetto LM, Mendlowicz MV, Romildo Bueno J. The validity of the Beck Depression Inventory-Short Form as a screening and diagnostic instrument for moderate and severe depression in medical inpatients. J Affect Disord. 2005;86(1): 87-91.
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35. Tucker WS, Armstrong CW, Gribble PA, Timmons MK, Yeasting RA. Scapular muscle activity in overhead athletes with symptoms of secondary shoulder impingement during closed chain exercises. Arch Phys Med Rehabil. 2010;91(4):550-556. 36. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86(2):420-428. 37. Calixtre LB, Nakagawa TH, Alburquerque-Sendín F, et al. Inter- and intra-rater reliability of 3D kinematics during maximum mouth opening of asymptomatic subjects. J Biomech. 2017;64:245-252. 38. Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15(2):155-163.
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39. Neziri AY, Scaramozzino P, Andersen OK, Dickenson AH, Arendt-Nielsen L, Curatolo M. Reference values of mechanical and thermal pain tests in a pain-free population. Eur J Pain. 2011;15(4):376-383. 40. Fillingim RB, King CD, Ribeiro-Dasilva MC, RahimWilliams B, Riley JL. Sex, gender, and pain: a review of recent clinical and experimental findings. J Pain. 2009;10(5): 447-485. 41. Calvo Lobo C, Romero Morales C, Rodríguez Sanz D, et al. Comparison of hand grip strength and upper limb pressure pain threshold between older adults with or without non-specific shoulder pain. Peer J. 2017;5: e2995.
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INTRODUCTION Shoulder pain is one of the most common causes of musculoskeletal pain,1,2 with impingement syndrome being the most frequent clinical condition.3 There is evidence that a
Department of Physical Therapy, Federal University of Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil. b Department of Sociosanitary Sciences, Radiology and Physical Medicine, University of Cordoba, Cordoba, Spain. c Maimonides Biomedical Research Institute of Cordoba (IMIBIC), Cordoba, Spain. Corresponding author: Catarina de Oliveira Sousa, PT, PhD, Departamento de Fisioterapia, Universidade Federal do Rio Grande do Norte, Av. Senador Salgado Filho, 3000, Campus Universitario, Lagoa Nova, Natal, RN, CEP 59.078-970, Brazil. (e-mail: [email protected]). Paper submitted December 17, 2018; in revised form April 24, 2019; accepted April 24, 2019. 0161-4754 © 2019 by National University of Health Sciences. https://doi.org/10.1016/j.jmpt.2019.04.002
participants with unilateral subacromial impingement syndrome (SIS) experience a decline in the pressure pain threshold (PPT),4 defined as a measure of pain sensitivity in response to force applied perpendicularly to the skin,5 suggesting a regional hyperalgesia process triggered by peripheral nociception resulting from tissue injury.4 The PPT has been widely used in clinical practice and studies to evaluate the response to treatment in different areas of the body and clinical conditions.4-10 However, pressure pain sensitivity seems to be different between muscles and not uniformly distributed in a same muscle,6,11 or even within an anatomic area.12 Moreover, errors by raters or participants can cause the measure to vary.13,14 The literature contains a number of PPT reliability studies that have shown good relative reliability for PPT measures, as assessed by the intraclass correlation coefficient (ICC), in clinical conditions such as epicondylalgia,15 knee osteoarthritis,10 cervical pain,6 and back pain.16,17 The
2
Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
ICC provides total data variability, but not what would be expected in trial-to-trial noise, which may be more suitable for monitoring clinical conditions. To that end, other analyses must be used to assess systematic changes or sampling errors that can occur owing to the variability of the equipment or method used, in addition to inherent biological variability.18 In this respect, Bland-Altman analysis assesses the systematic error and magnitude of the error that are clinically acceptable.19 In addition, it is essential to know the standard error of measurement (SEM) and the difference in measures where real change is attributable to a procedure or intervention, and not the assessment itself, which can be determined by the minimum detectable change (MDC).14 Both measures are necessary for adequate management of clinical conditions. Knowing relative and absolute reliability and how PPTs are present in different muscles will help the clinical management of SIS and contribute to understanding the peripheral4 and central sensitization9,20 process of the symptomatic participants. However, there is little information on the reliability of PPTs in upper limb muscles.6,12,13,21-24 The aim of the present study was to determine intraday intra- and interrater and interday intrarater reliability of PPT assessment in shoulder muscles, examining participants with symptoms of unilateral SIS and others asymptomatic for shoulder pain, and presenting error variance and MDC in the PPT of these assessments. We hypothesized that relative reliability would be good or excellent in all the assessments in both symptomatic and asymptomatic participants.
METHODS Design The reliability study occurred in 2 phases: the first included intraday intrarater and interrater reliability and the second included interday intrarater reliability. The study, conducted between May 2016 and October 2017, was approved by the Research Ethics Committee of the Federal University of Rio Grande do Norte (Protocol 1.529.040). All participants gave their informed consent after being advised of the objectives, risks, and benefits of the research. The present study followed the Guidelines for Reporting Reliability and Agreement Studies.25
Participants A total of 78 participants took part in the research. Fifty-two participants symptomatic for unilateral SIS were divided into 2 symptomatic groups (SG1 and SG2) with 26 participants in each one, and 26 asymptomatic participants were allocated in the asymptomatic group (AG) for unilateral SIS. The participants from SG1 and AG were
Journal of Manipulative and Physiological Therapeutics Month 2019
submitted to intraday intrarater assessment, where raters 1 and 2 evaluated the same participants on the same day. Only SG1 data were analyzed to assess interrater reliability. The SG2 was submitted to interday intrarater evaluation, where a same rater assessed the same participant on 2 different days. The symptomatic participants were recruited through flyers distributed at universities, gyms, and physical therapy and orthopedic clinics in the city and via social media. The symptomatic participants were allocated into SG1 and SG2 groups according to their availability to perform the assessment on 1 or 2 days. Asymptomatic participants were recruited from the student body and teaching staff of the local university through invitations. Table 1 shows sample characterization. The following inclusion criteria were adopted for the symptomatic participants: age between 18 and 60 years and history of unilateral shoulder pain for at least 1 month, regardless of the pain level, in the proximal anterolateral region,26 or C5 or C6 dermatomes,27 as determined by 3 of the following positive tests: Neer,28 Hawkins-Kennedy,29 Jobe,30 painful arc,3 external rotation resistance,31 Gerber, and Speed.32 The tests used to diagnose SIS usually exhibit high specificity or sensitivity, and the combination of these clinical tests is recommended to identify patients with SIS.3 The following exclusion criteria were established: bilateral SIS, adhesive capsulitis, history of symptom onset owing to trauma, multidirectional or anterior instability of the glenohumeral joint based on the inferior sulcus and positive grip tests, upper-extremity numbness and tingling, fibromyalgia or rheumatic disease, previous neck and shoulder surgery, systemic disease, body mass index (BMI) > 28 kg/m2, corticosteroid injection 3 months before evaluation or use of analgesics or muscle relaxants 72 hours before assessment, and depressive symptoms with a Beck Depression Inventory score 13.33,34 Asymptomatic participants did not present any inclusion or exclusion criteria exhibited for the symptomatic group, and they were matched for sex, age (±5 years), and BMI (±2 kg/m2) with symptomatic participants from SG1.
Raters and Training A digital mechanical pressure algometer (Wagner Instruments, Greenwich, Connecticut) was used to assess PPTs. This device consists of a 1-cm2 rubber disc connected to a pressure gauge, which displays values in kgf/cm2. Two raters with no clinical experience in evaluating PPTs participated in the study: a physical therapy student in the final year and a recently graduated physical therapist. Both raters underwent training to assess PPTs, to standardize the force applied in the algometer to reach a rate of 0.50 kgf/s, as previously described.6 To that end, training consisted of applying pressure on a rigid surface for
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Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
Table 1. Demographic Characteristics of All Participants Sex Age (y)
Symptomatic Group 1 (n ¼ 26)
Symptomatic Group 2 (n ¼ 26)
Asymptomatic Group (n ¼ 26)
P value
12 M; 14 F
16 M; 10 F
12 M; 14 F
.44
29 ± 17.50
35.12 ± 9.73
28 ± 17.50
.89
Height (m)
1.67 ± 0.07
1.67 ± 0.08
1.69 ± 0.09
.68
Weight (kg)
67.52 ± 8.93
68.4 ± 11.6
68.54 ± 11.70
.92
BMI (kg/m2)
24.26 ± 2.75
24.42 ± 2.52
23.99 ± 3.18
.92
6.19 ± 3.44
5.80 ± 0.86
3.50 ± 6.25
.11
Duration of symptoms (mo)
20.65 ± 21.88
19.48 ± 20.37
e
.52
Affected side (right/left)
20 D/6 ND
19 D/7 ND
e
.75
BDI (0/21)
Data are shown as frequency (sex, affected side), mean, and standard deviations (other data). BDI, Beck Depression Inventory; BMI, body mass index; D, dominant; F, female; M, male; ND, nondominant.
5 seconds. An application rate of approximately 2.50 ± 0.25 kgf was considered satisfactory.6 Training was coordinated by a physical therapist with 6 years of experience and totaled 5 hours per examiner.
Assessment Procedures The following muscles were assessed: lower trapezius (in the muscle belly, halfway between the midpoint of the medial border of scapula and the spinous process of the twelfth thoracic vertebra),35 upper trapezius (halfway between the C7 spinous process and acromion process), infraspinatus (in the muscle belly below the midpoint of the spine of scapula), and medial deltoid (muscle belly, near the inferolateral insertion).4 These muscles were selected for being related to scapular stabilization and positioning (upper and lower trapezius), belonging to the rotator cuff (infraspinatus), and being the primary motor in raising the arm in the scapular plane (medial deltoid). Only the affected side was assessed in participants with SIS, whereas the dominant side was evaluated in asymptomatic participants. All the points where pressure was applied with the digital algometer were previously marked by the physical therapist. Participants were assessed in the sitting position, with upper extremities relaxed and forearms resting on their thighs. For interrater and intrarater reliability, assessment was divided into 2 steps for both the SG1 and AG. In the initial step, one of the raters evaluated the participants, and after 5 minutes, the other did. Participants rested for 5 minutes between the first and second steps, which occurred similarly to the first. As such, each rater performed the same assessment twice, obtaining interrater and intrarater reliability on the same day. Two measuring circuits were performed for PPT measures, obtaining 1 measure in each circuit for each
muscle. The second circuit started as soon as the first one was completed. The sequence of muscle assessment and raters was conducted randomly using the website www. randomization.com, maintaining the same sequence in all the circuits, to ensure a constant period between the assessments of each muscle. To obtain interday intrarater measures, the SG2 was evaluated as described earlier, except the second step occurred 48 hours after the first, only on the affected side and assessed by only 1 rater (rater 2). Before starting the PPT assessment procedure, the participants were familiarized with the algometer, which consisted of a single evaluation in a muscle remote from those selected for assessment to ensure they understood the process. The pressure applied with the algometer occurred perpendicularly to the muscle fibers, and the following standard instruction was given: “I am going to start applying pressure to your muscle with this instrument. When the pressure becomes uncomfortable, say stop.”6 During measurements, the raters could not see the device’s display screen, and the PPT values were recorded by an experienced physical therapist.
Statistical Analysis The sample size was determined using Tama~no de la Muestra 1.1 software. Very good reliability was adopted (ICC 0.81)36 with variability of 0.2 and a ¼ 0.05,37 and a sample of 25 participants per group was estimated. Descriptive and inferential statistics were obtained using the SPSS statistical package, version 20.0 (IBM SPSS Statistics for Windows, IBM Corp., Armonk, NY). Means and standard deviations (SDs) were calculated for each variable. Sample distribution was assessed by applying the Shapiro-Wilk test. To investigate differences among groups for demographic and clinical data, 1-way analysis of
3
4
Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
variance (age, height, weight, BMI, and Beck Depression Inventory), c2 (sex), and Mann-Whitney U (symptom duration and affected side) tests were used, adopting a significance value of P < .05. For PPTs, the difference between the means of each assessment was calculated using the paired t and Wilcoxon tests for intrarater measures. Measures from the second assessment of each rater were used for interrater comparison. The ICC (ICC2,1) was calculated to estimate the relative reliability of intraday intrarater and interrater and interday intrarater measures.38 The ICC provides an estimate of population variances based on the variability in a particular set of measures.38 The ICC values less than 0.5 are indicative of poor reliability, values between 0.5 and 0.75 indicate moderate reliability, values between 0.75 and 0.9 indicate good reliability, and values greater than 0.90 indicate excellent reliability.38 Absolute reliability was estimated by calculating the SEM and MDC. The SEM indicates the standard error of the mean, and the MDC the value at which real change 14 occurred, in addition to the measurement pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi error. The SEM can be calculated by SD 1 ICC, and MDC by the formula MDC ¼ SEM √2. The SEM and MDC values were multiplied by 1.96 to obtain a 95% CI.6 To indicate the variation in absolute reliability, expressed in SEM percentage, the SEM%, obtained by MEAN 100, and MDC MDC%, by MEAN 100, were calculated,18 where the mean in the equation corresponds to all the data for the 2 test occasions (intrarater and intraday interrater or interday intrarater). Bland-Altman analysis was conducted to identify systematic biases and 95% limits of agreement (LOA) for each muscle19 using a dispersion graph of the differences and the means of assessments. The difference in mean (d) between the raters and the SD was quantified for this difference (SDd) to obtain 95% LOA. Next, d ± 1.96SDd was calculated, indicating the total error (bias and random error). If 0 is other than 95% LOA, there are systematic differences (biases) between the raters.15
RESULTS The demographic characteristics of participants belonging to the 3 groups are presented in Table 1. No intergroup difference was detected for any of the variables.
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good (0.90), as well as in the AG for both raters and all measures (ICC ¼ 0.91-0.98). Interrater reliability in SG1 was between good and excellent for all measures, with the ICC varying between 0.87 and 0.94. Regarding interday intrarater assessment, reliability was excellent for all the muscles assessed by rater 2, with an ICC between 0.95 and 0.96.
Absolute Reliability Table 3 shows the absolute reliability values. In general, intraday intrarater measures for the SG1 showed SEM95% between 0.43 and 0.75 kgf/cm2 and SEM% between 7.44% and 12.86%, and MDC95% between 0.60 and 1.06 kgf/cm2 and MDC% between 10.52% and 18.18%. For the AG, SEM95% varied from 0.61 to 1.50 kgf/cm2 and SEM% between 6.76% and 11.47%, and MDC95% from 0.87 to 2.12 kgf/cm2 and MDC% between 9.56% and 16.22%. Interrater reliability measures showed SEM95% values ranging from 0.58 to 0.77 kgf/cm2 and SEM% between 10.10% and 13.71%, and MDC95% from 0.82 to 1.08 kgf/ cm2 and MDC% between 14.29% and 19.39%. For interday intrarater measures, SEM95% varied between 0.61 and 0.82 kgf/cm2 and SEM% between 9.82% and 11.09%, and MDC95% from 0.86 to 1.16 kgf/cm2 and MDC% from 13.88% to 15.69%. The highest SEM95% , SEM%, MDC95%, and MDC% values for each assessment are highlighted in Table 3. Table 3 also shows the 95% LOA values for each muscle in intraday intrarater and interrater and interday intrarater assessment. The amplitude variation in intraday intrarater measures ranged from 1.56 to 3.44 kgf/cm2, for SG1 and AG, interrater between 2.32 and 2.86 kgf/cm2, and interday intrarater between 2.36 and 3.47 kgf/cm2. Figure 1 shows the Bland-Altman plots for rater 2 (intraday and interday intrarater assessments) and intraday interrater values, demonstrating that the difference in means is close to 0, with nonsignificant bias. In both intraday and interday intrarater assessments, bias was between -0.05 and 0.13, and interrater measures between 0.17 and 0.59. Outliers were present in more than 1 assessment (upper trapezius and infraspinatus muscles), and interday assessment values of the infraspinatus and medial deltoid muscles were more dispersed, although linear regression indicated no biased behavior in the variables.
DISCUSSION Relative Reliability Table 2 shows relative intraday intrarater and interrater and interday intrarater reliability. Comparisons of PPT measures in each assessment (intraday and interday; intraand interrater) revealed no difference. The intraday assessment reliability of SG1 was excellent for both raters (ICC ¼ 0.93-0.97) for all the muscles, with the exception of upper trapezius for rater 2, which was considered
As hypothesized, our study showed good or excellent reliability indices in intraday intrarater and interrater and interday intrarater assessments, indicating that algometry is a reliable assessment. We also present SEM and MDC values for intraday assessment and after 48 hours for symptomatic and asymptomatic participants, which could be used as reference values to help interpret PPT changes in interventions and clinical research.
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Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
Table 2. Relative Reliability of Pressure Pain Threshold for Intraday Intrarater and Interrater and Interday Intrarater Evaluations Groups
Upper Trapezius
Lower Trapezius
Infraspinatus
Middle Deltoid
ICC
0.95
0.95
0.93
0.96
95% CI
0.90-0.98
0.88-0.97
0.84-0.97
0.92-0.98
Assessment 1 (kgf/cm2)
2.57 ± 0.96
3.84 ± 1.26
3.71 ± 1.48
3.32 ± 1.36
3.70 (1.39)a
3.47 (1.47)a
2.92 (0.95)a
3.75 ± 1.35
3.62 ± 1.41
3.21 ± 1.33
3.55 (1.61)a
3.06 (2.09)a
2.85 (1.68)a
Intraday Intrarater SG1 (N ¼ 26) Rater 1
2.39 (0.67)a Assessment 2 (kgf/cm2)
2.44 ± 0.99 2.33 (0.94)a
P
.10
.40
.80
.25
ICC
0.90
0.96
0.95
0.97
95% CI
0.78-0.95
0.91-0.98
0.90-0.98
0.94-0.98
Assessment 1 (kgf/cm2)
2.30 ± 1.01
3.21 ± 1.25
3.40 ± 1.44
3.10 ± 1.35
2.91 (1.04)a
3.04 (1.41)a
2.80 (1.08)a
3.15 ± 1.23
3.41 ± 1.56
3.03 ± 1.33
3.07 (1.34)a
3.35 (1.37)a
2.80 (1.41)a
Rater 2
e Assessment 2 (kgf/cm2)
2.26 ± 0.87 e
P
.71
.63
.60
.27
ICC
0.95
0.92
0.95
0.91
95% CI
0.90-0.98
0.83-0.96
0.88-0.97
0.81-0.96
Assessment 1 (kgf/cm2)
3.03 ± 1.12
4.45 ± 1.52
4.44 ± 1.53
3.40 ± 1.20
e
4.42 (2.46)
e
4.47 ± 1.80
4.47 ± 1.80
3.29 ± 1.42
e
4.46 (2.75)a
e
AG (N ¼ 26) Rater 1
2.79 (1.54)a Assessment 2 (kgf/cm2)
3.09 ± 1.35 3.14 (2.01)a
P
.78
.87
.68
.44 (continued on next page)
The literature contains a number of PPT reliability studies showing that digital algometer assessment is reliable, exhibiting high ICC indices,1,6,20,22,38,39 as
observed in the present study. In addition to confirming measurement reliability, it is essential to understand its pattern under different conditions, to determine
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Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
Journal of Manipulative and Physiological Therapeutics Month 2019
Table 2. (continued) Groups
Upper Trapezius
Lower Trapezius
Infraspinatus
Middle Deltoid
ICC
0.98
0.95
0.97
0.96
95% CI
0.95-0.99
0.89-0.97
0.94-0.98
0.91-0.98
Assessment 1 (kgf/cm2)
2.79 ± 1.28
3.86 ± 1.55
3.84 ± 1.88
2.99 ± 1.33
e
3.67 (2.49)a
3.06 ± 1.28
3.98 ± 1.65
3.97 ± 1.98
e
e
3.83 (2.51)a
Rater 2
2.46 (1.70)a Assessment 2 (kgf/cm2)
2.80 ± 1.41 2.44 (1.93)a
P
.87
.41
.51
.51
ICC
0.87
0.89
0.93
0.94
95% CI
0.70-0.94
0.38-0.96
0.85-0.97
0.88-0.97
Intraday Interrater SG1 (N ¼ 26)
P
.59
.09
.58
.47
ICC
0.95
0.95
0.96
0.96
95% CI
0.90-0.98
0.90-0.98
0.92-0.98
0.91-0.98
Assessment 1 (kgf/cm2)
2.90 ± 1.47
3.53 ± 1.58
4.04 ± 2.12
3.28 ± 1.85
e
3.30 (2.55)a
2.43 (1.98)a
3.46 ± 1.57
4.00 ± 2.08
3.25 ± 1.82
e
3.45 (2.03)a
2.72 (1.80)a
Interday Intrarater SG2 (N ¼ 26)
2.30 (1.93)a Assessment 2 (kgf/cm2)
2.77 ± 1.36 2.30 (1.22)a
P
.92
.96
.98
.19
Values expressed as mean and standard deviation and used paired t test unless otherwise indicated. ICC, intraclass correlation coefficient; SG1, symptomatic group 1; SG2, symptomatic group 2. a Values expressed in median and range interquartile and used Wilcoxon test.
measurement variability in each clinical condition. To that end, it is important to verify the error variance between measures (LOA) in addition to the SEM and its MDC. Our LOA values show that amplitude varied from 1.56 kgf/cm2 to 2.94 kgf/cm2 in intraday intrarater (both raters) and interrater assessments, with the infraspinatus exhibiting the highest amplitude in interday assessment (2.36-3.47 kgf/cm2). Thus, although algometry is reproducible for shoulder muscles in participants symptomatic for SIS, our results suggest that clinical outcomes should be interpreted with caution. The variability of PPT measures may be explained by the different rate of pressure increase and reaction time of the
raters when asked to stop applying pressure.15 Additionally, the muscles evaluated in the present study have frequently been related to myofascial pain syndrome in participants with and without SIS,4,8,9 which causes peripheral sensitization provoked by continuous nociceptive afferents from the clinical condition.4 This may lead to more variable pain perception in these participants. Although training tends to minimize this problem, it is difficult to reproduce the same assessment condition because the muscles may resist differently to the applied pressure owing to the difference in tonus between them, and pressure pain sensitivity is likely not uniformly distributed between the muscle belly and tendons of the
Journal of Manipulative and Physiological Therapeutics Volume xx, Number xx
Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
Table 3. Absolute Reliability Indicators of Pressure Pain Threshold for Intraday Intrarater and Interrater and Interday Intrarater Assessments Groups
Upper Trapezius
Lower Trapezius
Infraspinatus
Middle Deltoid
Intraday Intrarater SG1 (N ¼ 26) Rater 1 SEM95% (kgf/cm2)
0.43
0.62
0.75
0.52
SEM%
8.43
8.27
10.23
8.06
MDC95% (kgf/cm2)
0.60
0.88
1.06
0.74
MDC%
11.92
11.70
14.47
11.40
LOA (kgf/cm2)
-0.65 to 0.91 (1.56)
-1.07 to 1.25 (2.32)
-1.38 to 1.56 (2.94)
-0.86 to 1.06 (1.92)
Rater 2 SEM95% (kgf/cm2)
0.58
0.48
0.65
0.45
12.86
7.67
9.79
7.44
0.82
0.68
0.92
0.64
MDC%
18.18
10.85
13.84
10.52
LOA (kgf/cm2)
-1.08 to 1.16 (2.24)
-0.90 to 1.01 (1.91)
-1.24 to 1.22 (2.46)
-0.76 to 0.88 (1.64)
SEM% MDC95% (kgf/cm2)
AG (N ¼ 26) Rater 1 SEM95% (kgf/cm2)
0.85
1.20
0.94
0.70
SEM%
9.38
10.50
9.67
11.47
MDC95% (kgf/cm2)
1.20
1.70
1.32
0.99
MDC%
13.27
14.85
13.67
16.22
LOA (kgf/cm2)
-1.11 to 1.01 (2.12)
-1.74 to 1.70 (3.44)
-1.61 to 1.49 (3.10)
-1.32 to 1.54 (2.86)
Rater 2 SEM95% (kgf/cm2)
0.61
1.02
0.66
1.50
SEM%
6.76
9.20
8.65
8.65
MDC95% (kgf/cm2)
0.87
1.45
0.93
2.12
MDC%
9.56
13.01
12.23
12.23
-1.33 to 1.07 (2.40)
-1.48 to 1.26 (2.74)
-1.08 to 0.96 (2.04)
LOA (kgf/cm2)
-0.74 to 0.72 (1.46)
(continued on next page)
same muscle.11,12 Intraparticipant reliability should also be considered because patient interpretation of discomfort may change, especially in interday assessments. These factors may be important sources for the different
PPT measures and should be considered in clinical assessment. Error and minimum change values can be interpreted using SEM% and MDC%, which provide variability data as
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Journal of Manipulative and Physiological Therapeutics Month 2019
Table 3. (continued) Groups
Upper Trapezius
Lower Trapezius
Infraspinatus
Middle Deltoid
Intraday Interrater SG1 (N ¼ 26) SEM95%(kgf/cm2)
0.66
0.63
0.77
0.58
13.71
11.62
10.78
10.10
0.93
0.89
1.08
0.82
MDC%
19.39
16.44
15.25
14.29
LOA (kgf/cm2)
-1.04 to 1.40 (2.44)
-0.59 to 1.77 (2.36)
-1.23 to 1.63 (2.86)
-0.99 to 1.33 (2.32)
SEM% MDC95%(kgf/cm2)
Interday Intrarater SG2 (N ¼ 26) SEM95% (kgf/cm2)
0.61
0.68
0.82
0.71
10.71
9.82
10.31
11.09
0.86
0.96
1.16
1.01
MDC%
15.15
13.88
14.57
15.69
LOA (kgf/cm2)
-1.05 to 1.31 (2.36)
-1.23 to 2.24 (3.47)
-1.48 to 1.54 (3.02)
-1.37 to 1.41 (2.78)
SEM% MDC95% (kgf/cm2)
AG, asymptomatic group; LOA, limits of agreement; MDC, minimum detectable change; SEM, standard error of measurement; SG1, symptomatic group 1; SG2, symptomatic group 2.
Fig 1. Bland-Altman plots for rater 2 (intraday and interday intrarater assessments) and intraday interrater values. The dashed line represents the bias and the solid line represents the limits of agreement.
Journal of Manipulative and Physiological Therapeutics Volume xx, Number xx
a function of the absolute value of the variable, expressed in percentage. As such, considering shoulder muscles, the variation of these measures is generally less than 15% in most intraday intrarater assessments, with only 2 exceptions (upper trapezius in SG1, rater 2, and middle deltoid in AG, rater 1), whereas in intraday interrater and interday intrarater assessments, the variation was greater, but still less than 20%. Thus, change must be at least 20% of MDC% to be deemed meaningful. Nevertheless, there is no acceptable agreement regarding these measures, that is, whether these slight differences could significantly affect clinical practice. The highest SEM95%, MDC95%, SEM%, and MDC% values in Table 3 are similar for all the muscles in both symptomatic and asymptomatic participants, but the latter obtained higher values. Moreover, our results show higher values than those of a previous reliability study. We found SEM95% and MDC95% values of 0.53 and 0.82 kgf/cm2, respectively, for the upper trapezius, whereas Walton et al6 reported 0.41 and 0.58 kgf/cm2. These differences may be related to the sources of PPT measurement variability previously mentioned. In summary, the present study presents PPT values for the shoulder muscles that may contribute to clinical practice. However, the results should be interpreted with caution because error intervals and minimum clinical change can vary between examiners and assessments. As such, we underscore the need for each examiner to know their own absolute reliability as a function of the population under study. The present study exhibits a number of limitations, such as not being able to divide the sample according to sex and age group to assess possible differences between men and women and age range. Although some studies have reported that women have a lower PPT40 and that the aging process also provokes this decline,41 there is still no consensus, especially regarding reliability measures.40 Further, the participants were not categorized for pain intensity, which could provide information on the relation between tissue irritability and reliability. Finally, the current study did not allow knowing how the clinical experience of the raters and participants might affect these measures. Studies that bridge these gaps could lead to more adequate use of the PPT.
Nascimento et al Reliability of Pressure Pain Threshold in Shoulder Muscles
FUNDING SOURCES
This study provides evidence that the relative reliability of PPT assessment is good or excellent in intraday intrarater and interrater and interday intrarater evaluations in participants symptomatic for unilateral SIS and their asymptomatic counterparts. Moreover, absolute reliability values related to raters (intrarater or interrater), participants’ clinical condition, and sequence of assessments (intraday and interday) may be useful as references when interpreting PPT measurements in participants symptomatic or asymptomatic for SIS.
CONFLICTS
OF INTEREST
The first author received a master scholarship from CAPES e Brazilian Federal Agency for Support and Evaluation of Graduate Education within the Ministry of Education of Brazil during the conduct of the study. No conflicts of interest were reported for this study.
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): J.D.S.N., C.O.S., F.A.S. Design (planned the methods to generate the results): J.D.S.N., C.O.S., F.A.S. Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): J.D.S.N., C.O.S. Data collection/processing (responsible for experiments, patient management, organization, or reporting data): J.D.S.N., W.F.O., L.P.V. Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): J.D.S.N., C.O.S., F.A.S., L.P.V., W.F.O. Literature search (performed the literature search): J.D.S.N., C.O.S. Writing (responsible for writing a substantive part of the manuscript): J.D.S.N., C.O.S., F.A.S. Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): C.O.S., F.A.S.
Practical Applications
CONCLUSION
AND
The relative reliability of PPTs in the shoulder muscles is, overall, excellent for both symptomatic and asymptomatic participants for shoulder pain. The error intervals and MDCs of PPTs of shoulder muscles are provided. Error intervals and MDC values provided can be used to interpret PPT measures in shoulder muscles in interventions and clinical research. The findings should be interpreted with caution, given that error intervals and MDCs could vary depending on the rater and assessments, as well as sex or age of the participants.
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Journal of Manipulative and Physiological Therapeutics Month 2019
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