Relationships between the fibromyalgia impact questionnaire, tender point count, and muscle strength in female patients with fibromyalgia: A cohort study

Abstract

Objective

To test the hypothesis that fibromyalgia (FM) patients with reduced lower extremity strength are more symptomatic and tender than FM patients with normal muscle strength.

Methods

A total of 840 FM patients and 122 healthy subjects were evaluated between 1998 and 2005. All of the patients completed version 1 of the Fibromyalgia Impact Questionnaire (FIQ) and were assessed for tender points and knee muscle strength. All subjects underwent bilateral isokinetic knee muscle strength testing in flexion and extension. Normative knee muscle strength values were calculated from the healthy subjects, and the FM cohort was divided in 2 groups: 1) patients with normal muscle strength and 2) patients with low muscle strength (2 SDs below normal). The clinical characteristics of these 2 groups were compared.

Results

Significantly reduced knee muscle strength was found in 52% of the patients. There were no clinically significant differences between patients with low versus normal muscle strength. There were no clinically significant correlations between total FIQ score, tender point count, and muscle strength. Only 4.6% of the FIQ scores and 5.1% of the tender point counts were explained by muscle strength.

Conclusion

Significantly reduced knee muscle strength was found in more than half of the patients. Patients with subnormal muscle strength were not more symptomatic or tender than patients with normal muscle strength. There were no clinically significant correlations between FIQ, tender point count, and muscle strength; therefore, reduced knee muscle strength appears to be a common objective abnormality in FM that is independent of measurements of disease activity. The implication of this finding in regard to the clinical assessment of FM needs further study.

INTRODUCTION

Fibromyalgia (FM) is a generalized pain syndrome that is also characterized by reduced functional capacity and fatigue (1–4). The combined effect of FM symptoms often has a significant impact on the activities of daily living and work capacity of patients, resulting in large socioeconomic expenses (5, 6). The combination of pain and reduced physical capacity may lead to inactivity and a vicious circle may be created, leading to progressive deconditioning. One component of deconditioning is reduced muscle strength, which has been proven to be a valid predictor for reduced physical function in many diseases and disorders, e.g., in the elderly (7) and in patients with rheumatoid arthritis (8, 9), osteoarthritis (10), and stroke (11). Muscle strength has been examined several times in patients with FM and is reduced compared with healthy subjects (4, 12–26). Muscle strength is usually measured from knee extensors and flexors, and only a few studies have reported the results of muscle strength of upper body muscle groups. However, it is still not clear what roles motivation, pain, and supraspinal centers play in determining the extent of reduced muscle strength in FM. Also, muscle strength has most frequently been reported in middle-aged patients, and little is known about muscle strength in older patients with FM. Muscle strengthening interventions have been applied in patients with FM, showing that the neuromuscular system is trainable in FM (27) and increased muscle strength has significant effects on physical function in patients with FM (28). In experimental studies, musculoskeletal pain has been shown to cause reduced muscle function during both maximal (29) and submaximal (30) contractions, as well as during functional activities such as walking (31), lunging (32), and stair climbing (33). Taking into account the chronic pain situation as in FM, it was surmised that reduced muscle strength may be related to some FM symptoms. The specific purpose of this study was to test the hypothesis that, compared with healthy controls, FM patients with reduced knee muscle strength are more symptomatic and tender than FM patients with normal muscle strength.

The functional component of the Fibromyalgia Impact Questionnaire (FIQ) has been criticized for containing activities that are not habitual and aiming at severe disability, causing a potential floor effect (34, 35). It has not been evaluated to what extent information in the FIQ reflects physical impairment.

The tender point count is currently the accepted clinical evaluation of FM severity, which is based on localized pain on palpation in at least 11 of 18 selected muscle–tendon junctions or tender points (36). The tender point count is under criticism for lacking objectivity, and its relationship with the underlying pathophysiology is uncertain (35, 37). Objective measures of physical function would be of value in the clinical assessment of FM severity and could provide useful guidance for interventions.

In this respect, obvious questions that need to be addressed are whether information on reduced muscular function in an FM population is contained in the available instruments for assessing disease severity, and whether they are self-reported or clinical. The present study is a cross-sectional study of an FM cohort compared with reference material of healthy subjects.

PATIENTS AND METHODS

Patients.

The patient sample was comprised of 925 female patients referred to the Department of Rheumatology at Frederiksberg Hospital from 1998 to 2005 and subsequently diagnosed with FM according to the 1990 American College of Rheumatology (ACR) criteria (36). Patients that were diagnosed with FM and had concomitant diagnoses potentially affecting their muscle strength measures (i.e., arthritis, osteoarthritis, lumbar or cervical intervertebral discus prolapse, whiplash and other musculoskeletal disorders, cerebral hemorrhage, embolisms and other neurologic disorders, and psychiatric diagnoses) did not have their muscle strength measured. This yielded a total of 840 female patients with FM who were evaluated for knee muscle strength, FIQ scoring, and number of ACR tender points (Table 1).

Table 1. Demographic data and observed values of the FM cohort and the control group*

	N	Mean ± SD	Median	95% EI
* FM = fibromyalgia; 95% EI = 95% empirical (data distribution) interval; BMI = body mass index; FIQ = Fibromyalgia Impact Questionnaire.
FM cohort
Age, years	840	46.0 ± 9.3	46.7	28.5–65.1
Height, meters	840	1.65 ± 0.07	1.65	1.52–1.80
Weight, kg	840	72.1 ± 15.4	70.0	49.0–106.1
BMI, kg/m^2	840	26.4 ± 5.4	25.6	18.7–39.4
FIQ score	721	63.0 ± 16.1	62.7	32.2–92.6
FIQ physical function item	721	5.4 ± 2.3	5.9	0.3–8.9
Tender point count	828	17.2 ± 1.6	18.0	12.0–18.0
Control group
Age, years	126	51.6 ± 16.8	53	18.6–84.5
Height, meters	126	1.63 ± 6.9	163.1	149.5–176.5
Weight, kg	126	67.0 ± 11.3	64.9	44.9–89.1
BMI, kg/m^2	126	25.2 ± 4.5	24.5	16.4–34.1

Healthy reference subjects.

Isokinetic knee muscle strength data from 122 healthy women were extracted from an ongoing study of normative muscle strength values at The Parker Institute. These participants were recruited through a random selection from the Copenhagen City Heart Study (38). From 10,135 attendees at examination, the Copenhagen City Heart Study randomly selected 305 women. Exclusion criteria consisted of musculoskeletal problems, cardiac disease with impaired physical performance, prior central nervous system involvement, or the presence of an active disease requiring treatment by a physician. Following the given criteria, 296 women received a written invitation to participate in the study. A total of 126 women (42.6%) responded positively and 122 participated in the knee measurements (Table 1).

Fibromyalgia Impact Questionnaire.

The original FIQ (39, 40) was used to assess the status of FM as reported by patients with FM. The FIQ is based on patient self-report and is the most frequently used available instrument for obtaining a standardized measure for patient-reported disease severity (35). The FIQ is a validated instrument developed to measure FM patient status, progress, and outcomes. It has been designed to measure the components of health status believed to be the most affected by FM, including questions related to physical function (39). The FM patients filled out the FIQ on the same day as the clinical examination (diagnosis) and the muscle strength test. A total of 721 FM patients returned a valid FIQ.

Tender point count.

The number of tender points was determined according to the ACR standard (36) using manual palpation. A total of 828 patients with FM had a valid registration of a tender point count.

Isokinetic knee muscle strength.

Valid isokinetic knee muscle strength was available from 733 of the included patients. To define the patients' maximal isokinetic muscle strength, we used 2 different isokinetic dynamometers: the Lido Active (Lido Multi Joint II; Loredan, Davis, CA) and the Biodex System 3 pro set (Biodex Medical Systems, Shirley, NY). A study comparing these 2 dynamometers showed no clinically relevant difference between them (41). The dynamometer is made from a motor that moves a test arm with a constant speed (isokinetic) throughout the range of motion (ROM). The system registers the resisting torque against the test arm exerted by the patient and a computer records torque, velocity, and the angular position. From the recorded torque, the peak (maximum) value was extracted as the result. The reliability and validity of the Biodex have been examined previously (41, 42). The dynamometer was warmed up and calibrated on a daily basis before measurements.

The isokinetic knee muscle strength test consisted of 3 repetitions on both the right and left sides in both directions (flexion and extension), and was performed throughout the study period by the same 2 experienced and specially designated laboratory technicians following a standardized protocol. The standard test in our clinic encompassed strength tests at angular velocities of 30°/second and 60°/second. In the last part of the study period, to make the strength testing protocol more comprehensive, we decided to add a test at 90°/second, and 266 of the FM patients underwent this advanced protocol. The ROM was from 15–95° of knee flexion (0° = full extension). The patient was seated comfortably in the isokinetic testing device and strapped to the chair with unelastic shoulder straps and a body belt. The lower part of the test leg was placed in the foot support so that the axis of the rotation of the device corresponded to the axis of knee flexion and extension. The axis for the flexion/extension was assumed to pass through the medial and lateral femoral epicondyles. The patients were asked to extend and flex their knee with maximal effort and force.

During the tests, the patients were given verbal encouragement as well as visual feedback from the Lido or Biodex computer monitor in an attempt to achieve a maximal effort level (43, 44). The peak value across the 3 repetitions was chosen to reflect the maximal concentric isokinetic knee muscle strength for a given direction (flexion or extension) and angular velocity (30°/second, 60°/second, or 90°/second). The coefficient of variation (CV) between the 3 repetitions was calculated for each patient.

Statistical analyses.

The primary analysis tested the hypothesis that, compared with healthy controls, FM patients with reduced muscle strength in knee extension and flexion are more symptomatic and tender than FM patients with normal muscle strength. Data from the 122 healthy subjects were analyzed using a multidimensional normal distribution regression model, yielding estimates of predicted normative muscle strength values based on height, weight, and age, including a between-subjects variation estimate. Subsequently, predicted normative muscle strength values in the FM cohort were calculated and predicted muscle strength was plotted against observed values (Figure 1). Each patient was classified as being either within (MS_norm) or below (MS_low) normal muscle strength. To be classified as having reduced muscle strength (MS_low), an FM patient had to fall below the predicted muscle strength by −1.96 × SD in both flexion and extension and at 30°/second, 60°/second, and 90°/second. Based on this dichotomization, unpaired t-tests were used to compare the measures of disease severity (FIQ [total and single item], FIQ physical function item [total and single item], and tender point count), age, height, weight, and body mass index (BMI) between FM in the MS_norm and MS_low subgroups.

Figure 1. Scatter plots of the relationships between observed and predicted isokinetic knee muscle strength in the fibromyalgia cohort at different angular velocities and movement directions. Solid lines show the identity line (y = x); broken lines show 1.96 × SD of the normative values based on the between-subjects variation from the regression model.

To (re)test the hypothesis that FM patients as a population have reduced muscle strength, paired-sample t-tests were computed in order to test if the observed muscle strength in the FM cohort was reduced compared with the predicted normative muscle strength based on the regression analyses.

To test the relationships between knee muscle strength and self-reported and clinical measures of disease severity in the FM cohort, bivariate correlations and stepwise linear regression analyses were used to test the relationships between the measures of FM severity (FIQ, FIQ physical function item, and tender point counts) and the isokinetic knee muscle strength measures.

RESULTS

Disease severity measures.

Summaries of the cohort demographics together with FIQ scores, FIQ physical function item scores, and tender point counts are shown in Table 1. There was a significant mean difference in age, with the MS_low subgroup being 4.4 years older than the MS_norm subgroup (P < 0.0001). The mean height of the MS_low subgroup was 1.5 cm lower than that of the MS_norm subgroup (P = 0.002). No significant differences were observed in weight and BMI between the 2 subgroups (P = 0.75 and P = 0.09, respectively).

Muscle strength.

The observed and predicted knee muscle strength in the FM cohort were averaged across the left and right knees (Table 2). The muscle strength data are also shown by age decades in Figure 2. The paired-sample t-tests comparing observed and predicted knee muscle strength values showed that the observed muscle strength in the FM patients was significantly lower than the predicted normative values (P < 0.000001). The CVs of the measurements are also shown in Table 2. Depending on angular velocity, the average CV of the FM patients was from 13.2–17.0, which was higher than that of the healthy controls (5.6–6.9).

Table 2. Observed and predicted isokinetic knee muscle strength values in the fibromyalgia cohort together with the observed muscle strength values for the healthy women recruited from the Copenhagen City Heart Study*

	N	Mean ± SD	Median	95% EI	CV
* Values were averaged across the left and right knees. 95% EI = 95% empirical (data distribution) interval; CV = coefficient of variation; Nm = newton meters; N/A = not applicable.
Observed muscle strength, Nm
Extension 30°/second	733	98.6 ± 39.4	100.0	20.7–184.9	14.9
Flexion 30°/second	733	47.6 ± 20.9	47.0	10.65–90.4	17.0
Extension 60°/second	732	83.8 ± 36.3	86.5	15.1–157.8	13.2
Flexion 60°/second	732	41.7 ± 19.0	41.5	8.5–79.9	15.0
Extension 90°/second	266	74.2 ± 31.5	75.5	15–138.9	13.2
Flexion 90°/second	266	36.9 ± 17.3	36.9	6.6–71.4	16.0
Predicted muscle strength, Nm
Extension 30°/second	733	142.5 ± 18.0	139.4	120.2–195.6	N/A
Flexion 30°/second	733	80.1 ± 10.2	77.9	69.1–111.0	N/A
Extension 60°/second	732	132.7 ± 17.5	130.1	109.0–180.7	N/A
Flexion 60°/second	732	74.4 ± 9.7	72.3	63.4–102.5	N/A
Extension 90°/second	266	118.8 ± 17.2	115.2	95.6–171.8	N/A
Flexion 90°/second	266	68.1 ± 9.6	66.1	57.1–101.9	N/A
Control group, Nm
Extension 30°/second	122	117.2 ± 23.0	127.5	72.1–162.2	6.4
Flexion 30°/second	122	65.3 ± 13.7	66.3	38.5–92.1	6.9
Extension 60°/second	122	110.2 ± 21.7	112.5	67.7–152.6	5.8
Flexion 60°/second	122	61.8 ± 12.3	64.0	37.7–85.9	6.2
Extension 90°/second	122	97.5 ± 19.0	101.3	60.2–134.7	5.6
Flexion 90°/second	122	57.2 ± 11.1	58.8	35.3–79.0	6.2

Figure 2. Bar charts of observed and predicted normative isokinetic knee muscle strength at different angular velocities and movement directions in the female fibromyalgia patients, divided into age groups based on decades. Number of patients in each age group: 20–29, n = 29; 30–39, n = 168; 40–49, n = 274; 50–59, n = 223; 60–69, n = 33; 70–79, n = 6. Error bars show the 95% confidence interval. Nm = newton meters.

Main analysis.

The relationship between the observed and predicted knee muscle strength results is shown in Figure 1. The dichotomization of the FM cohort resulted in 48.4% of the cohort being classified as having subnormal MS (MS_low) in both flexion and extension and at all angular velocities, and 51.6% were classified as having normal MS (MS_norm).

There was a statistically (but not clinically) significant difference in tender point count (P = 0.009), with the MS_low subgroup having 0.3 more tender points than the MS_norm subgroup. There were no differences in the FIQ or FIQ physical function item scores between the MS_low and MS_norm subgroups (P = 0.39 and P = 0.22, respectively). No differences between the MS_low and MS_norm subgroups were found in the analysis of any of the single-item FIQ scores (P > 0.21). The physical function single-item scores in the MS_low subgroup had significantly lower scores than the MS_norm subgroup in the questions relating to “do laundry” (mean difference 0.16 points) and “drive a car” (mean difference 0.25 points; P = 0.04 for both).

Correlations.

The correlations between the FIQ, FIQ physical function item, tender point count, and muscle strength are shown in Table 3. All correlations were statistically significant at P < 0.001. Similar correlations were found in both the MS_low and MS_norm subgroups and in all age groups.

Table 3. Matrix of correlation coefficients (Pearson's r) between the FIQ, FIQ physical function item, tender point count, and isokinetic muscle strength in the fibromyalgia cohort*

	FIQ	FIQ physical function item	Tender point count
* All correlations are statistically significant at P < 0.001. FIQ = Fibromyalgia Impact Questionnaire.
Tender point count	0.158	0.125	–
Muscle strength extension
30°/second	−0.212	−0.212	−0.172
60°/second	−0.232	−0.242	−0.179
90°/second	−0.180	−0.175	−0.197
Muscle strength flexion
30°/second	−0.188	−0.233	−0.166
60°/second	−0.194	−0.250	−0.167
90°/second	−0.187	−0.204	−0.212

Regression analyses.

For the total FIQ score, 4.6% variation was explained by isokinetic knee muscle strength (R² = 0.046, root mean square error [RMSE] = 239.3; P = 0.069). The regression analysis of the FIQ physical function item showed that 5.1% of the FIQ physical function variation was explained by knee muscle strength (R² = 0.051, RMSE = 0.46; P = 0.045). Similarly, 5.1% of the tender point count variation was explained by knee muscle strength (R² = 0.051, RMSE = 3.04; P = 0.026). The detailed coefficient estimates are shown in Table 4.

Table 4. Coefficient estimates, RMSEs, and P values associated with the multivariate regression models*

	FIQ	FIQ physical function item	Tender point count
* Values are the estimate ± SEM. RMSE = root mean square error; FIQ = Fibromyalgia Impact Questionnaire.
Intercept	67.8 ± 2.8	1.8 ± 0.1	17.9 ± 0.3
Slope extension 30°/second	0.034 ± 0.08	0.001 ± 0.004	−0.002 ± 0.01
Slope flexion 30°/second	−0.062 ± 0.15	−0.005 ± 0.006	−0.007 ± 0.02
Slope extension 60°/second	−0.010 ± 0.12	0.004 ± 0.005	−0.002 ± 0.01
Slope flexion 60°/second	−0.201 ± 0.22	−0.008 ± 0.009	−0.007 ± 0.02
Slope extension 90°/second	−0.027 ± 0.11	−0.003 ± 0.005	0.002 ± 0.012
Slope flexion 90°/second	0.106 ± 0.19	0.001 ± 0.008	−0.005 ± 0.02
RMSE	239.3	0.46	3.04
P (full model)	0.069	0.045	0.026
R^2	0.046	0.051	0.051

Sensitivity analyses.

There were no differences in either of the muscle strength variables between patients with and without a valid FIQ or tender point count (FIQ P > 0.48 and tender point count P > 0.39). Also, there were no differences in the FIQ between patients with and without valid muscle strength measurements (P = 0.39) and valid tender point counts (P = 0.21). A statistically significant difference in tender point count between patients with and without valid muscle strength measurements was observed (P = 0.008), but this is unlikely to be clinically significant because patients with valid muscle strength measurements had only 0.3 more tender points (95% confidence interval 0.1–0.5) than those without valid muscle strength measurements.

DISCUSSION

The present study of a large cohort of patients with FM demonstrated that FM patients as a population have reduced lower extremity isokinetic muscle strength compared with normative values. Although this may hold true in study samples, this study shows that on a population scale, approximately 50% of the present FM cohort can be classified as having knee muscle strength within normative ranges (with respect to height, weight, and age). The comparison of the clinical characteristics of these 2 groups (MS_low and MS_norm) revealed only sparse and randomly distributed differences of rather small magnitudes, i.e., there is very limited correlation of knee muscle strength and items contained in the FIQ. Similarly, there is very limited correlation of knee muscle strength and tender point counts. The current data are limited to the lower extremities, whereas muscle strength in other muscle groups may or may not be affected in patients with FM. A reduced grip strength has been documented by several groups (14, 17, 19), although there is some controversy over the strength of the elbow joint; Miller et al (45) found normal values, whereas in a smaller group of FM patients we found indications of a reduction (26).

The limited information about knee muscle strength contained in the self-reported and clinical measures of disease may be a result of only 2 lower extremity activities included in version 1 of the FIQ (“walk several blocks” and “do yard work”). However, neither of these 2 questions showed differences between the MS_low and MS_norm subgroups. Although we administered the original version of the FIQ (40), an updated version exists (online at http://www.myalgia.com/FIQ/FIQ_D.pdf). The updated version of the FIQ (version 2) has a question related to stair climbing, which would be of relevance to this study. Also, most of the tender points are in the upper body and the relationship between upper body tender point counts and upper body muscle strength remains to be clarified.

When measuring muscle strength in patients with FM, a higher variability between maximal isokinetic contraction trials (CV) has been observed in FM (26). A high variability, expressed as the CV, may indicate a poor ability to perform a maximal muscle contraction, i.e., the CV may be an indicator of effort (46). The CV in the present study is similar to earlier observations in patients with FM (26) and somewhat lower than that in patients with low back pain (47), which may indicate that patients with FM have difficulties producing maximal strength reliably. Although this variation in itself may have some importance for compliance with interventions, e.g., exercise, no associations between the CV and other items were found in our statistical analysis.

There are no standards for measurement of muscle strength in FM, and different studies have applied different muscle strength test protocols. However, the present muscle strength values compare well with previous studies (25, 48), and regardless of methodology, muscle strength may be suggested as a further measurement to describe FM function. The present material is uniquely large and the observed muscle strength may be used as a reference for upcoming studies.

In our material, no measurement of physical activity was given, although the answers on the FIQ indicated very low levels. Normal values for patients with FM have been found in 2 studies of aerobic capacity (19, 26) despite the reduced muscle strength reported in both studies. It may be speculated that FM leads to a relatively more pronounced reduction in type 2 fibers, which has indeed been described in biopsy studies (49).

Reduced muscle strength has a major impact on disability in patients with rheumatoid arthritis (8, 9) and osteoarthritis (10), and is a predictor of risk of falling in the elderly (50). For instance, increased falls and imbalance have recently been reported in patients with FM (51), and it would be reasonable to study their relationship with reduced lower extremity muscle strength. Although the present study is cross-sectional, any possible prognostic value of knee muscle strength in FM patients remains to be clarified. It may be speculated that differences in muscle strength could be of importance in choosing therapy modalities. In general, strengthening exercise is advocated in patients with FM, whereas this may not be quite as relevant in patients with normal muscle strength.

Based on our results, the measurements of muscle strength in patients with FM describe an extra dimension of the disease that is not covered by the clinical instruments that are commonly used. Quadriceps and hamstring muscles are important contributors to walking performance, and lower extremity muscle strength is an important predictor of walking performance (7). One limitation of this study is that there was no evaluation of ambulation, such as the 6-Minute Walk Test.

In conclusion, the present study shows that FM patients with reduced muscle strength in knee extension and flexion compared with healthy controls of comparable age are not more symptomatic and tender than FM patients with normal muscle strength. Although knee muscle strength is generally reduced, half of the FM patients have knee muscle strength values within the predicted normative reference range. The associations between self-reported and clinical measures of disease severity and knee muscle strength among FM patients are weak. This implies that the measurement of muscle strength represents a separate feature that may or may not be reduced in FM, and that knowledge of muscle strength cannot be derived from clinical or self-reported measures of FM symptoms. Finally, the present results on more than 500 patients with FM may be useful as a reference.

AUTHOR CONTRIBUTIONS

All authors were involved in drafting the article or revising it critically for important intellectual content, and all authors approved the final version to be published. Dr. Bliddal had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Study conception and design. Dreyer, Danneskiold-Samsøe, Bliddal.

Acquisition of data. Lund, Dreyer, Danneskiold-Samsøe.

Analysis and interpretation of data. Henriksen, Lund, Christensen, Jespersen, Bennett, Danneskiold-Samsøe, Bliddal.