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Men With Late Effects of Polio Decline More Than Women in Lower Limb Muscle Strength: A 4-Year Longitudinal Study
1 2 3 4 5 PM R XXX (2015) 1-9 www.pmrjournal.org 6 7 8 9 10 11 12 13 14 15 16 17 Q2 18 19 20 21 22 23 24 Abstract 25 26 27 Background: In persons with prior paralytic poliomyelitis, progressive muscle weakness can occur after a stable period of at least 28 15 years. Knowledge is limited about which factors influence changes in lower limb muscle strength in these persons. 29 Objective: To assess changes in lower limb muscle strength annually over 4 years in persons with late effects of polio and to 30 31 identify prognostic factors for changes in muscle strength. 32 Design: A prospective, longitudinal study. 33 Setting: University hospital outpatient program. 34 35 Q1 Participants: Fifty-two ambulant persons (mean age standard deviation: 64 6 years) with verified late effects of polio. 36 Methods: Mixed linear models were used to analyze changes in muscle strength and to identify determinants among the following 37 covariates: gender, age, age at acute polio infection, time with late effects of polio, body mass index, and estimated baseline 38 muscle weakness. 39 40 Main Outcome Measurements: Knee extensor and flexor and ankle dorsiflexor muscle strength were measured annually with a 41 Biodex dynamometer. 42 Results: The men (n ¼ 28) had significant linear change over time for all knee muscle strength measurements, from 1.4% (P < 43 44 .05) per year for isokinetic knee flexion in the less-affected lower limb to 4.2% (P < .001) for isokinetic knee extension in the 45 more-affected lower limb, and for 2 ankle dorsiflexor muscle strength measurements (3.3%-1.4% per year [P < .05]). The women 46 (n ¼ 24) had a significant linear change over time only for ankle dorsiflexor measurements (4.0%-5.5% per year [P < .01]). Gender 47 was the strongest factor that predicted a change in muscle strength over time. 48 49 Conclusions: Over 4 years, men had a greater decline in muscle strength than did women, but the rate of decline did not 50 accelerate. This finding indicates that gender could be a contributing factor to the progressive decline in muscle strength in 51 persons with late effects of polio. 52 53 54 55 56 57 58 In healthy men and women (aged 50-70 years), the Introduction 59 predicted decline in knee and ankle dorsiflexor muscle 60 strength is 1%-2% per year [14]. A decline in muscle In persons with a history of an acute paralytic polio61 62 strength also occurs over time in persons with late myelitis infection, new symptoms are experienced by 63 effects of polio, but the rapidity of this decline is 28%-64% after a stable period of at least 15 years [1,2]. 64 65 unclear. In a review from 2005 (including 17 articles These new symptoms are referred to as “late effects of 66 with sample sizes from 12-103 participants) most polio” or “postpolio syndrome” [3] and often include 67 studies showed a slow rate of decline in muscle muscle weakness, general fatigue, muscle pain, and/or 68 69 strength over time [15], with approximately 7% over joint pain [1,4-6]. These symptoms can lead to reduced 70 4 years and 15% over 8 years [16-19]. Thereafter, few mobility in daily activities such as walking, standing, 71 72 studies have assessed the decline in lower limb muscle and climbing stairs [7-9]. Progressive decline in muscle 73 strength in persons with late effects of polio [20-23]. strength is an underlying cause of the reduced mobility 74 75 The decline in muscle strength in those studies is [10,11] and is likely to increase when these persons 76 reported to be between 1% and 3% [20,22,23], except acquire additional disabilities [12,13]. 77 78 79 1934-1482/$ - see front matter ª 2015 by the American Academy of Physical Medicine and Rehabilitation 80 http://dx.doi.org/10.1016/j.pmrj.2015.05.005
Original Research
Men With Late Effects of Polio Decline More Than Women in Lower Limb Muscle Strength: A 4-Year Longitudinal Study ˚rdh, PT, PhD, Vibeke Horstmann, Sc lic, Ulla-Britt Flansbjer, PT, PhD, Christina Broga Jan Lexell, MD, PhD
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Muscle Strength and Late Effects of Polio
for one study that reported a larger and more progressive decline (5%-8% per year) [21]. Very few studies have assessed prognostic factors for the decline in muscle strength in persons with late effects of polio. One study showed that men declined more rapidly in isokinetic knee extensor strength than did women [11]. Wille ´n et al [23] found that the decline in muscle strength over 4 years was higher in persons who were stronger at the baseline assessment. In a recent study, Bickerstaffe et al [20] showed that persons with higher isometric maximal voluntary contraction (MVC) at baseline had a greater decline in strength over 10 years. Even though previous studies have evaluated the decline in muscle strength over time in persons with late effects of polio, they differ with regard to study design and the statistical methods used. To analyze longitudinal data in order to identify potential determinants, the mixed-random and fixed effect regression models (mixed linear models; MLM) are recommended [24-26]. To our knowledge, no study has used the MLM model to assess changes in muscle strength over time in persons with late effects of polio. The main aim of this study was to assess changes in strength in the knee extensor and flexor muscles and ankle dorsiflexor muscles annually over 4 years in persons with late effects of polio. The second aim was to identify determinants of changes in muscle strength, such as gender, age, age at acute polio infection, length of time with new symptoms, body mass index (BMI), and estimated baseline weakness. Methods Participants Fifty-two community-dwelling ambulant persons were recruited from a postpolio rehabilitation clinic at a university hospital in the south of Sweden. Inclusion criteria were (1) 50-75 years of age; (2) a confirmed history of acute poliomyelitis affecting the lower limbs, with new weakness after a period of functional stability of at least 15 years; and (3) ability to walk at least 300 m with or without an assistive and/or orthotic device. Exclusion criteria were (1) using a wheelchair as the main mode of transportation and (2) ongoing major depression, systemic disease, or any other disease that could affect muscle strength. The treating physician selected participants who met the inclusion and exclusion criteria and were mildly to moderately affected in their lower limbs. These persons were invited consecutively to participate in the study in connection with their regular follow-up visits to the clinic. We aimed for at least 50 participants to obtain a reasonably large sample that could be assessed annually over the 4-year period. Inclusion continued for 18 months (2007 to 2009) until 52 persons had agreed to participate.
For all 52 participants, an electromyogram had been recorded in the lower limbs (vastus lateralis and tibialis anterior muscles) as part of the initial routine clinical examination and verification of prior polio, and there were no other diseases that could explain their new symptoms. According to the National Rehabilitation Hospital (NRH) Post-Polio Limb Classification [27], all participants had postpolio NRH class II to V (indicating clinically stable or unstable polio) in at least one of their knee or ankle dorsiflexor muscles. According to each person’s own perception of his or her muscle weakness, one lower limb was defined as the “more-affected limb” and the other lower limb that was less affected or not affected was defined as the “less-affected limb.” Prior to inclusion in the study, information about the purpose of the study was provided, and each individual gave his or her written informed consent to participate. The study followed the principles of the Helsinki declaration. Muscle Strength Measurements Isokinetic concentric knee extension, knee flexion, and ankle dorsiflexion muscle strength and isometric knee extension and ankle dorsiflexion muscle strength were measured with a Biodex Multi-Joint System 3 PRO dynamometer (Biodex Medical Systems, Shirley, NY) using a standard protocol developed in our research group [28,29]. These studies have shown that lower limb muscle strength can be reliably measured in persons with late effects of polio (for knee extensors and flexors, intraclass correlation coefficients [ICC2,1] ranging from 0.85-0.99 and standard error of measurement [SEM] from 10.2-13.9 Newton meter [Nm], and for ankle dorsiflexors, ICC2,1 ranging from 0.85-0.99 and SEM from 2.5-3.7 Nm). Before each strength measurement, the range of motion was set and the Biodex software applied the gravity correction. For the knee muscle strength measurements, the participants were seated in the adjustable chair of the dynamometer without shoes or an orthotic device and were stabilized with straps across the shoulders, waist, and thigh. After a structured warm-up the participants performed 3 maximal isokinetic extensor and flexor contractions at 60 /s, and the highest peak torques were recorded (in Nm). After a 2-minute rest, the participants performed 2 maximal isometric knee extensor muscle contractions with a knee flexion angle at 90 , and the highest MVC was recorded (in Nm). For the ankle dorsiflexor strength measurements, the participants were seated in the adjustable chair of the dynamometer, with the leg elevated by a support arm just above the knee with the angles of the hip at 90 flexion and the knee joints at 30 flexion. The ankle was placed and secured on the Biodex footplate. To warm up and become familiar with the ankle dorsiflexor strength measurements, 3-5 submaximal contractions with the dorsiflexor muscles were performed. After a 1-minute
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rest, 3 maximal contractions at 30 /s were performed, with 30 seconds rest between each contraction. Each contraction started from a relaxed plantar-flexed position without any preload, and the highest peak torques were recorded (in Nm). After a 2-minute rest, testing continued with 2 maximal isometric contractions with a 60-second rest between each contraction. The ankle was fixed in 10 plantar-flexed position, and the highest MVC was recorded (in Nm). Procedures All strength measurements were performed by the same physiotherapist (U-BF). The participants were tested annually over 4 years (a total of 5 times) and as close as possible to 1 year between each test. The knee muscle strength was measured before the ankle dorsiflexor muscle strength, and the strength of the less-affected lower limb was measured before that of the more-affected lower limb. Consistent verbal encouragement was given throughout the tests. The total time for the strength measurements at each test session was approximately 1 hour. After completion of the annual test sessions, a summary of the test results was given to the participants. Statistics Data from the muscle strength measurements provided 10 quantitative variables for the analyses: 4 knee extension and 2 knee flexion strength measurements and 4 ankle dorsiflexor strength measurements. Of the 52 participants, 1 participant missed 1 test session the third year and another 3 participants missed the last 2 or 3 test sessions. The missing values were compensated for in the statistical model. Because of weakness and/or stiffness, 30 participants were unable to perform the ankle dorsiflexor strength measurements with the more-affected lower limb, and 6 participants were unable to do so with the less-affected lower limb. The statistical analyses for the ankle dorsiflexors were therefore based on 22 participants for the moreaffected lower limb and on 46 participants for the less-affected lower limb. The characteristics of the sample were described by frequencies, means, and standard deviations (SDs). Differences between men and women at baseline were analyzed by independent samples t-tests. For each participant, the predicted muscle strength for isometric knee extension and ankle dorsiflexion was calculated based on gender, age, height, and body mass specific values for a healthy population [14]. These values were used to calculate the predicted muscle weakness at baseline (ie, the differences between the predicted and the measured muscle strength values). MLM [26] were used for the longitudinal data analyses. Estimated means and SDs of all muscle strength measurements were obtained based on the covariance
3
matrix. The fixed linear effects (mean values for the group), the random effects (individual variations around the mean) and the deviations from the linear slopes over the 4 years were calculated for men and women, respectively. To analyze prognostic determinants for any changes in muscle strength, the independent variables (covariates) gender, age, age at acute polio, length of time with new symptoms, BMI, and the predicted baseline weakness in isometric muscle strength were analyzed in the mixed linear regression models. First, all covariates and their interaction with time were inserted into the models. The nonsignificant predictors were then removed in a backward manner, starting with the least significant interaction term; no covariate was removed when the interaction term was statistically significant. The final models contained only covariates where the covariate itself or its interaction with time was significant. All interval scaled variables used in the analyzes were centered to the mean, giving positive covariate values for the participants above the mean values of age, age at acute polio, time with new symptoms, BMI, and baseline weakness. The gender variable was coded 0 (women) and 1 (men). All calculations were performed using SPSS statistics software version 21.0 (IBM Corp, Armonk, NY). The significance of random effects was tested with the deviance test (2 degrees of freedom [df]) based on restricted maximum likelihood. Significance levels below .05 represent statistical significance. Results In Table 1, the characteristics of the 52 participants (28 men and 24 women) are presented. Their mean age at the study enrollment was 64 years (SD 6, range 5274), and the mean time since onset of new symptoms was 13 years (SD 7, range 2-28). Fifty-two percent were most affected in their right lower limb, and 71% had verified prior polio in both lower limbs. Walking aids were used by 10% of the participants and ankle foot orthoses were used by 19%. The mean time between each test session was close to 1 year (12.1 months, SD 0.8), and the participants were all free from acute illnesses and injuries at each testing session. At baseline the men were significantly stronger than the women in all knee muscle strength measurements and for the less-affected lower limb regarding ankle dorsiflexor strength, and thus data for the men and women were analyzed separately. Linear Trends and Random Effects in Muscle Strength Over Time In Tables 2 and 3, time from baseline and the estimated means and SDs at each test occasion over the
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Muscle Strength and Late Effects of Polio
The men experienced a significant fixed linear decline over time for all knee muscle strength measurements, ranging from 1.0 to 4.5 Nm/y (from 1.4% [P <.05] per year for the less-affected isokinetic knee flexion to 4.2% [P < .001] for more-affected isokinetic knee extension; Table 2). For the ankle dorsiflexors, a significant fixed linear effect of time was found only for isokinetic muscle strength in the more-affected limb and for isometric muscle strength in the less-affected limb, ranging from 0.82 to 0.42 Nm/y, respectively (3.3%-1.4% per year [P < .05]). The random effect of time was significant for all strength measurements of the less-affected limb, as well as for isokinetic measurements of the more-affected limb (deviance [df ¼ 2]: 7.7 (P < .05) to 14.6 [P < .01]). For the women (Table 3), no significant fixed linear decline over time was observed for the knee muscle strength measurements. There was a significantly increased isometric ankle dorsiflexor muscle strength (P < .01) for both the less-affected lower limbs (0.71 Nm/y; 4.0%) and the more-affected lower limbs (0.87 Nm/y; 5.5%), but no significant fixed linear effect of time for isokinetic ankle dorsiflexor strength measurements. A significant random effect of time was found for 3 of the strength measurements in the lessaffected limb (isokinetic knee extensors and isokinetic and isometric ankle dorsiflexors; deviance [df ¼ 2] 7.8 [P < .05] to 13.3 [P < .01]), but no significant random effect was found for the more-affected limb. Over the 4 years, no significant deviation from the linear slopes occurred for any strength measurement, either for the men or for the women, indicating that the change in muscle strength over time did not accelerate.
Table 1 Characteristics of the 52 participants with late effects of polio Characteristic
Values
Gender Men Women Age, y BMI Age at acute polio infection, y Time with new symptoms, y Most-affected leg Right Left Both lower limbs affected by polio Walking aid None Stick or crutch Rollator Orthotic device None Ankle-foot orthosis Baseline isometric weakness, Nm* Less-affected knee extension More-affected knee extension Less-affected ankle dorsiflexors More-affected ankle dorsiflexors
28 24 64 26 5 13
(54) (46) (6); 52-74 (3); 21-37 (4); 0-15 (7); 2-28
27 (52) 25 (48) 37 (71) 47 (90) 4 (8) 1 (2) 42 (81) 10 (19) 66 115 18 11
(50); (51); (12); (10);
40-250 40-251 3-39 10-43
Values are represented as n (%) or mean (SD); range. SD ¼ standard deviation; BMI ¼ body mass index; Nm ¼ Newton meter. * For each participant the baseline isometric weakness was calculated as the difference between the predicted muscle strength based on age, gender, length, and body weight specific values for a healthy population [14] and the measured muscle strength value.
4 years, along with the fixed linear effects for the group and the random effects for the individuals, are presented for men and women, respectively.
Table 2 Estimated mean of strength measurements for knee extensors, knee flexors, and ankle dorsiflexors (Newton meter) in 28 men with late effects of polio Estimated Mean of Fixed Effects Test Assessment Less-affected lower limb Knee extensors isokinetic 60 /s Knee flexors isokinetic 60 /s Knee extensors isometric MVC Ankle dorsiflexors isokinetic 30 /s§ Ankle dorsiflexors isometric MVC§ More-affected lower limb Knee extensors isokinetic 60 /s Knee flexors isokinetic 60 /s Knee extensors isometric MVC Ankle dorsiflexors isokinetic 30 /s{ Ankle dorsiflexors isometric MVC{
Baseline
After 1 y
After 2 y
After 3 y
After 4 y
Fixed Linear Effect
Random Effect†
130.1 71.0 158.4 28.8 30.6
(9.0) (5.0) (10.6) (2.2) (2.7)
130.6 73.4 155.0 28.6 30.0
(9.0) (5.0) (10.6) (2.2) (2.7)
124.4 70.8 147.4 28.0 30.8
(9.1) (5.0) (10.6) (2.2) (2.7)
123.4 67.7 140.7 28.7 31.4
(9.1) (5.0) (10.6) (2.2) (2.7)
122.2 68.7 143.3 28.4 32.1
(9.1) (5.0) (10.6) (2.2) (2.7)
2.30** 1.00* 4.47*** 0.06‡ 0.42
9.8** 12.7** 8.4* 10.2** 14.6**
91.0 51.0 96.3 24.6 24.0
(9.2) (4.8) (10.7) (3.3) (4.0)
91.3 52.3 95.6 26.3 23.9
(9.2) (4.8) (10.7) (3.3) (4.0)
84.4 49.7 93.6 23.9 23.6
(9.2) (4.8) (10.7) (3.3) (4.0)
81.7 46.8 86.1 22.6 22.8
(9.3) (4.9) (10.7) (3.3) (4.0)
76.5 48.3 86.6 22.3 23.6
(9.3) (4.9) (10.7) (3.3) (4.0)
3.83*** 1.07* 2.85*** 0.82* 0.18‡
8.6* 7.7* 1.06‡ 12.6** 1.9‡
Estimated values are presented as mean (SD). SD ¼ standard deviation; MVC ¼ maximal voluntary contraction. *P < .05. **P < .01. ***P < .001. † Deviance (df ¼ 2). ‡ Not significant. § Participants able to perform the measurements: n ¼ 24. { Participants able to perform the measurements: n ¼ 12. FLA 5.2.0 DTD PMRJ1488_proof 27 May 2015 11:55 am ce
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721 722 723 Estimated Mean of Fixed Effects 724 725 Baseline After 1 y After 2 y After 3 y After 4 y Test Assessment Fixed Linear Effect Random Effect† 726 727 Less-affected lower limb 728 Knee extensors isokinetic 60 /s 81.8 (6.1) 80.8 (6.1) 77.9 (6.1) 80.7 (6.1) 80.9 (6.1) 0.19‡ 7.8* 729 Knee flexors isokinetic 60 /s 40.3 (3.0) 42.7 (3.0) 42.1 (3.0) 41.4 (3.0) 44.4 (3.0) 0.68‡ 2.4‡ 730 ‡ ‡ Knee extensors isometric MVC 92.9 (6.9) 86.0 (6.9) 86.1 (6.9) 85.2 (6.9) 86.4 (6.9) 1.38 5.8 731 Ankle dorsiflexors isokinetic 30 /s§ 19.5 (1.4) 20.2 (1.4) 20.3 (1.4) 19.7 (1.4) 19.6 (1.4) 0.04‡ 13.3** 732 733 Ankle dorsiflexors isometric MVC§ 17.7 (1.6) 18.1 (1.6) 18.8 (1.6) 19.5 (1.6) 20.6 (1.6) 0.71** 9.5** 734 More-affected lower limb 735 Knee extensors isokinetic 60 /s 59.0 (6.2) 61.9 (6.2) 58.9 (6.2) 58.4 (6.2) 58.7 (6.2) 0.43‡ 1.1‡ 736 ‡ ‡ Knee flexors isokinetic 60 /s 25.4 (2.9) 26.0 (2.9) 26.2 (2.9) 26.0 (2.9) 27.8 (2.8) 0.47 1.7 737 Knee extensors isometric MVC 61.0 (6.8) 62.7 (6.8) 61.7 (6.8) 60.1 (6.8) 60.8 (6.8) 0.30‡ 0.7‡ 738 739 Ankle dorsiflexors isokinetic 30 /s{ 16.8 (2.5) 16.8 (2.5) 17.5 (2.5) 17.3 (2.5) 17.0 (2.5) 0.10‡ 3.9‡ 740 Ankle dorsiflexors isometric MVC{ 15.9 (2.4) 19.1 (2.4) 17.2 (2.4) 20.4 (2.4) 19.6 (2.4) 0.87** 2.8‡ 741 Estimated values are presented as mean (SD). 742 743 SD ¼ standard deviation; MVC ¼ maximal voluntary contraction. 744 *P < .05. 745 **P < .01. 746 Q3 ***P < .001. 747 † Deviance (df ¼ 2). 748 ‡ 749 Not significant. § 750 Participants able to perform the measurements: n ¼ 22. { 751 Participants able to perform the measurements: n ¼ 10. 752 753 754 Discussion Determinants of Change in Muscle Strength Over 755 756 Time 757 This longitudinal study over 4 years found that men 758 759 with late effects of polio declined more in muscle All covariates and interactions with time that were 760 strength than did women. Men had a significant effect significantly related to knee muscle strength are pre761 over time for all knee muscle strength measurements sented as the final model in Table 4. The strongest in762 763 and for 2 of the ankle dorsiflexors muscle strength fluence was found for the participants’ gender; the 764 measurements (P < .05 to P < .001). Women had a sigdecline in strength over time was significantly larger for 765 766 nificant effect only for the isometric ankle dorsiflexor the men than for the women for all knee muscle 767 strength measurements. No significant deviations from strength measurements in the more-affected lower limb 768 the linear slopes occurred over the 4 years. The stronand for the knee flexor strength in the less-affected 769 770 gest prognostic determinant for the decline in muscle lower limb. Among the other covariates, the only 771 strength was the participants’ gender. interaction with time was found for the more affected 772 773 Several factors may explain the differences between isokinetic knee extensor strength measurements. 774 the results in the present and previous studies. In the Younger persons, those who have had new symptoms for 775 776 present study, we found a decline in knee muscle a longer time, and those with less baseline weakness 777 strength measurements for men (4.5% and 1.8% per declined more in muscle strength, even though the in778 year) but no significant linear trend for any of the knee teractions with time were quite small. 779 780 muscle strength measurements for women. Instead, we All covariates and the interactions with time that 781 found a significant positive linear trend for isometric were significantly related to ankle dorsiflexor muscle 782 783 ankle dorsiflexor strength measurements. Contrary to strength are presented as the final model in Table 5. 784 previous studies [11,20,21,23], our population consisted The strongest influence was found for the participants’ 785 of roughly equal proportions of men and women (54% gender; the men were significantly stronger at baseline 786 787 men). The balanced gender distribution made it possible in both the less- and more-affected lower limb. The 788 for us to analyze if there were any differences for the men only interaction with time was for isokinetic dorsi789 790 and the women in muscle strength over 4 years. In other flexion in the more-affected lower limb; the decline in 791 studies [20,21,23] the measurements for men and women muscle strength was significantly larger for the men 792 were combined, and only one study has shown that men than for the women. For all other covariates, there 793 794 decline more rapidly in muscle strength than women with were only 2 minor interactions with time in the more 795 regard to isokinetic knee extension strength [11]. affected ankle dorsiflexor measurements, namely, 796 797 The characteristics of the participants could also those with more baseline weakness and older persons. 798 have influenced the results. Many studies of persons These participants had declined more in muscle 799 800 with late effects of polio were published between 1994 strength over time.
Table 3 Estimated mean of strength measurements for knee extensors, knee flexors and ankle dorsiflexors (Newton meter) in 24 women with late effects of polio
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6
Table 4 Knee muscle strength measurements and the final models with covariates and interaction with time for the total sample
Less-affected lower limb Isokinetic extensors Isokinetic flexors Isometric MVC extensors More-affected lower limb Isokinetic extensors Isokinetic flexors Isometric MVC extensors
Age‡
Age *Time
BMI
BMI *Time
Age Acute Polio
Age Acute Polio *Time
Intercept
Trend
Gender†
Gender *Time
80.0 39.2 90.5
1.3§ 0.7§ 3.0**
54.1*** 35.4*** 72.7***
e 1.8* e
1.5* 1.1* e
e e e
e e 2.0*
e e e
2.3* 2.2** e
e e e
42.0 18.4 41.5
0.6§ 0.5§ 0.3§
69.6*** 40.2*** 76.5***
4.9*** 1.6* 2.6*
1.4* 0.9* 1.2*
0.2* e e
e e 2.4*
e e e
e 1.4* e
e e e
PPS
PPS *Time
Less Aff Weakness
Less Aff Weakness *Time
More Aff Weakness
More Aff Weakness *Time
e e
e e
0.6*** 0.2*** 0.8***
e e e
e e e
e e e
0.2§ e e
0.2* e e
0.1* 0.1** 0.2**
e e e
0.9*** 0.3*** 1.0***
0.03* e e
Table 5 Ankle dorsiflexor muscle strength measurements and the final models with covariates and interaction with time for the total sample
Age‡
Age *Time
Age Acute Polio
Age Acute Polio *Time
BMI
BMI *Time
PPS
PPS *Time
Less Aff Weakness
Less Aff Weakness *Time
More Aff Weakness
More Aff Weakness *Time
Intercept
Trend
Gender†
Gender *Time
19.4 16.1
0.1§ 0.5**
9.9*** 14.3***
e e
e e
e e
e e
e e
e e
e e
e e
e e
0.7*** 0.9***
e e
e e
e e
14.2 12.3
0.6§ 0.1§
13.5*** 14.7***
1.4** e
e 0.2§
e 0.1*
e
e
e e
e e
e e
e e
e e
e e
0.8*** 0.9***
0.1** e
{
Less-affected lower limb Isokinetic strength Isometric MVC More-affected lower limb# Isokinetic strength Isometric MVC
Intercept and trend for the significant factors in the final model for each strength measurement. BMI ¼ body mass index; PPS ¼ time with late effects of polio; less aff weakness ¼ baseline weakness for less-affected isometric knee extensor muscle strength; more aff weakness ¼ baseline weakness for more-affected isometric knee extensor muscle strength; MVC ¼ maximal voluntary contraction. *P < .05. **P < .01. ***P < .001. † Woman is reference category. ‡ Baseline age. § Not significant. { Participants able to perform the measurements: n ¼ 46. # Participants able to perform the measurements: n ¼ 22.
Muscle Strength and Late Effects of Polio
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Intercept and trend for the significant factors in the final model for each strength measurement. BMI ¼ body mass index; PPS ¼ time with late effects of polio; less aff weakness ¼ baseline weakness for less-affected isometric knee extensor muscle strength; more aff weakness ¼ baseline weakness for more-affected isometric knee extensor muscle strength; MVC ¼ maximal voluntary contraction. *P < .05. **P < .01. ***P < .001. † Woman is reference category ‡ Baseline age. § Not significant.
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and 1998 [11,16-19]. In the present study the participants were generally older (mean age 64 years) compared with other studies, where the mean age was around 50 years [11,16-18,20,21]. Even if the participants in this study were older, no deviations from the linear slopes occurred over the 4 years, and age explained only a small additional part of the linear trend. Thus, it seems that the decline in muscle strength in older persons with late effects of polio is fairly stable. Furthermore, in previous studies, isometric knee extension strength has been the most common measurement, and the values at baseline have varied between 57 and 176 Nm [11,16,18,20]. In many studies only one limb has been measured [16-18,20], so the isometric knee extension muscle strength can be a measure of either the more or the less affected lower limb, and therefore the strength values are not comparable with those of our study. Another factor that might have influenced the results is the outcome measurement used. To be able to follow muscle strength over time, reproducible and sensitive measurement tools are needed. For many years manual muscle testing and a handheld dynamometer have been used to measure muscle strength in persons with late effects of polio. However, these measurements are less reproducible and sensitive than isokinetic dynamometry [30,31]. In this study we used isokinetic dynamometry, which is currently the recommended measurement tool to evaluate changes in muscle strength over time [32,33]. Furthermore, the test protocols were standardized and carefully followed at each test session. Other factors that could have influenced the result are the frequency of strength measurements and the length of follow-ups. In our study, all participants were measured annually over 4 years, the minimum follow-up time suggested for persons with late effects of polio [15]. In most previous studies the follow-up times have varied between 4 and 10 years [16-18,20,21,23], but only 2 studies have performed the measurements annually [18,21]. If the follow-up time is short, long-term changes are difficult to estimate; on the other hand, if annual measurements are performed, a progressive decline in muscle strength can more easily be detected. In one study with annual follow-ups, including 23 persons with late effects of polio (stable and unstable; ie, those with new weakness) and 14 healthy control subjects [18], no significant differences in the mean change in muscle strength (the slope of the lines) for the 3 groups were found over a 7-year period. In the other study [21], a large decline in strength occurred over 5 years. Isokinetic knee muscle strength at 60 /s declined 7.8% for the extensors and 5.1% for the flexors per year with a progressive decline in strength over time. However, the progressive decline was not significant, probably because of a large number of dropouts; only 8 of the 76 baseline limb measurements were repeated during the entire period. In our study, almost all participants
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performed every test session, and no significant change of the slope over time was found, indicating that the change in muscle strength was similar over time. The statistical method used also could have influenced the results. We used the MLM models, which are recommended for longitudinal clinical studies [24-26]. The MLM technique takes into account the correlation between the measures obtained in the same persons, as well as missing observations. The MLM combines the effect of average time with any individual variation over time (linear trends, random effects, and changes in the slope). To be able to calculate deviations from the linear slopes over time, at least 3 measurement points are required [25]. In previous follow-up studies in persons with late effects of polio, older and more traditional statistical methods have been used to analyze the longitudinal data, and most participants have only been measured twice. To our knowledge, this study is the first using the MLM in a longitudinal study of the annual decline in muscle strength in persons with late effect of polio. Few studies [11,20,23] have analyzed potential prognostic factors for a change in muscle strength. In this study, we formed a model with covariates and identified different significant factors that could explain parts of the outcome for the strength measurements. The covariatesdgender, age, and BMIdwere chosen because they are of importance when calculating normal values for muscle strength [14]. The final model showed that gender was the strongest predictor for the effect of time and only for isokinetic knee extensors in the more affected lower limb; baseline weakness together with age and time with new symptoms could explain a small additional part of the linear trend. In a study by Wille ´n et al [23], the decrease in muscle strength was higher in persons who were stronger at the baseline assessment for both isokinetic knee flexion and ankle dorsiflexion. In another study, men declined more rapidly in knee extensor strength than did women, but only for isokinetic strength [11]. Taken together, more studies are needed to control for the effect of gender. There might be other factors not used in our model with covariates, such as pain, fatigue, physical activity, or the size of motor units at baseline, that could explain the differences between men and women [4,34-36] . Strengths and Limitations Only 4 persons missed 1 to 3 test sessions during the 4 years (altogether, 8 out of a total of 260), which could be considered a very low dropout rate, especially because the statistical model compensated for the missing values. Both lower limbs were measured and the less affected limbs in 15 participants were “almost” healthy because they did not have any polio-related weakness in that limb. Even though persons with late effects of polio are a heterogeneous group, the paresis in the lower limb can differ within the limb, as well as between limbs. In addition, the weakness in one lower
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Muscle Strength and Late Effects of Polio
limb has probably had an influence on the other limb during mobility-related activities since childhood. In this study, we measured knee muscle strength and ankle dorsiflexor strength. Strength measurements in these muscles have been shown to be reproducible using a Biodex dynamometer [28,29]. Other muscle groups, such as the hip extensors and flexors, could have been selected because they are also related to gait performance. However, our clinical experience is that they are less affected in persons with late effect of polio and therefore they were not measured. Furthermore, these muscles are more difficult to measure isokinetically than knee extensors, knee flexors, and ankle dorsiflexors, and no data are available on the reproducibility of isokinetic measurements of these muscles in persons with late effects of polio. For ankle muscle strength measurements, the variation over time was hardly significant. However, few participants (n ¼ 22) could perform measurement of their more-affected ankle dorsiflexors; several participants had a pronounced weakness in this muscle group and were therefore unable to perform any active movement in the ankle. On the other hand, 46 of the participants were able to perform the ankle dorsiflexor measurements in the less-affected lower limb, and there were no discernible differences between the more-affected and the lessaffected lower limb. The positive linear trends for the ankle dorsiflexor muscles for both men and women are somewhat surprising but could be due to the fact that we had a selected group of participants or due to a learning effect. A small nonsignificant learning effect has been reported in a previous test-retest reliability study [28], and the technique to perform the measurements might be improved when repeated several times. In future research other measurement modes, such as passive modes, might be more useful in very weak muscles. Overall, we found small changes in muscle strength over time, which could be due to both the study sample and the length of follow-up. Not enough data are available to perform a comprehensive power analysis, because gender differences have not been the primary aim of previous studies of changes in muscle strength in persons with late effect of polio. A sample size of 52 persons could be considered small, but annual data collection is very time consuming for both participants and assessors. It is important that the assessments be performed regularly and by the same assessor following a strict protocol. We chose to follow up the participants for 4 years because this period has been recommended as the minimum follow-up time for persons with late effects of polio [15]. Compared with previous studies with annual measurements [18,21], and taking into account the very low dropout rate in this study, we still believe the number of participants to be satisfactory for this type of analysis. All participants were ambulant and had mild to moderate late effects of polio. They were weaker in the ankle dorsiflexors than in their knee muscles, and this weakness
was compensated for by an ankle-foot orthosis in 10 participants, but no one needed a knee-ankle-foot orthosis. Thus the results in this study are limited to persons with mild to moderate disability. In future studies a larger sample with a wider range of disability, as well as a longer follow-up period, would be desirable. However, some of the participants in this study were already quite old (at the last test session the oldest person was 78 years), and a reduction in muscle strength will probably continue in both men and women as a result of normal aging [37]. Conclusion Small changes in muscle strength were seen in persons with late effects of polio over 4 years. The strongest predictor of change in lower limb muscle strength was the participants’ gender. Men declined more in muscle strength than did women, especially in the knee muscles, but the rate of the decline did not accelerate over time, which indicates that gender could be a contributing factor to the progressive decline in muscle strength in persons with late effects of polio. References 1. Farbu E, Gilhus NE, Barnes MP, et al. EFNS guideline on diagnosis and management of post-polio syndrome. Report of an EFNS task force. Eur J Neurol 2006;13:795-801. 2. Trojan DA, Cashman NR. Post-poliomyelitis syndrome. Muscle Nerve 2005;31:6-19. 3. Halstead LS, Rossi CD. New problems in old polio patients: Results of a survey of 539 polio survivors. Orthopedics 1985;8:845-850. 4. Jensen MP, Alschuler KN, Smith AE, Verrall AM, Goetz MC, Molton IR. Pain and fatigue in persons with postpolio syndrome: Independent effects on functioning. Arch Phys Med Rehabil 2011; 92:1796-1801. 5. Boyer FC, Tiffreau V, Rapin A, et al. Post-polio syndrome: Pathophysiological hypotheses, diagnosis criteria, drug therapy. Ann Phys Rehabil Med 2010;53:34-41. 6. Lexell J, Broga ˚rdh C. Life satisfaction and self-reported impairments in persons with late effects of polio. Ann Phys Rehabil Med 2012;55:577-589. 7. Broga ˚rdh C, Flansbjer UB, Espelund C, Lexell J. Relationship between self-reported walking ability and objectively assessed gait performance in persons with late effects of polio. NeuroRehabilitation 2013;33:127-132. 8. Horemans HL, Bussmann JB, Beelen A, Stam HJ, Nollet F. Walking in postpoliomyelitis syndrome: The relationships between timescored tests, walking in daily life and perceived mobility problems. J Rehabil Med 2005;37:142-146. 9. Wille ´n C, Sunnerhagen KS, Ekman C, Grimby G. How is walking speed related to muscle strength? A study of healthy persons and persons with late effects of polio. Arch Phys Med Rehabil 2004;85: 1923-1928. 10. Laffont I, Julia M, Tiffreau V, Yelnik A, Herisson C, Pelissier J. Aging and sequelae of poliomyelitis. Ann Phys Rehabil Med 2010;53:24-33. 11. Agre JC, Grimby G, Rodriquez AA, Einarsson G, Swiggum ER, Franke TM. A comparison of symptoms between Swedish and American post-polio individuals and assessment of lower limb strengthda four-year cohort study. Scand J Rehabil Med 1995;27: 183-192. 12. Bartels MN, Omura A. Aging in polio. Phys Med Rehabil Clin N Am 2005;16:197-218.
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U.-B. Flansbjer et al. / PM R XXX (2015) 1-9 13. Bouza C, Munoz A, Amate JM. Postpolio syndrome: A challenge to the health-care system. Health Policy 2005;71:97-106. 14. Harbo T, Brincks J, Andersen H. Maximal isokinetic and isometric muscle strength of major muscle groups related to age, body mass, height, and sex in 178 healthy subjects. Eur J Appl Physiol 2012; 112:267-275. 15. Stolwijk-Swuste JM, Beelen A, Lankhorst GJ, Nollet F. The course of functional status and muscle strength in patients with lateonset sequelae of poliomyelitis: A systematic review. Arch Phys Med Rehabil 2005;86:1693-1701. 16. Grimby G, Kvist H, Grangard U. Reduction in thigh muscle crosssectional area and strength in a 4-year follow-up in late polio. Arch Phys Med Rehabil 1996;77:1044-1048. 17. Grimby G, Stalberg E, Sandberg A, Sunnerhagen KS. An 8-year longitudinal study of muscle strength, muscle fiber size, and dynamic electromyogram in individuals with late polio. Muscle Nerve 1998;21:1428-1437. 18. Rodriquez AA, Agre JC, Franke TM. Electromyographic and neuromuscular variables in unstable postpolio subjects, stable postpolio subjects, and control subjects. Arch Phys Med Rehabil 1997;78:986-991. 19. Stalberg E, Grimby G. Dynamic electromyography and muscle biopsy changes in a 4-year follow-up: Study of patients with a history of polio. Muscle Nerve 1995;18:699-707. 20. Bickerstaffe A, van Dijk JP, Beelen A, Zwarts MJ, Nollet F. Loss of motor unit size and quadriceps strength over 10 years in post-polio syndrome. Clin Neurophysiol 2013;125:1255-1260. 21. Saeki S, Hachisuka K. Change in lower limb isokinetic muscle strength of polio survivors over 5-year follow-up. J UOEH 2009;31:131-142. 22. Sorenson EJ, Daube JR, Windebank AJ. A 15-year follow-up of neuromuscular function in patients with prior poliomyelitis. Neurology 2005;64:1070-1072. 23. Wille ´n C, Thoren-Jonsson AL, Grimby G, Sunnerhagen KS. Disability in a 4-year follow-up study of people with post-polio syndrome. J Rehabil Med 2007;39:175-180. 24. Hoffman L, Stawski R. Persons as context: Evaluating betweenperson and within-person effects in longitudinal analysis. Res Hum Dev 2009;6:97-120.
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25. Locascio JJ, Atri A. An overview of longitudinal data analysis methods for neurological research. Dement Geriatr Cogn Dis Extra 2011;1:330-357. 26. Edwards LJ. Modern statistical techniques for the analysis of longitudinal data in biomedical research. Pediatr Pulmonol 2000;30: 330-344. 27. Halstead LS, Gawne AC, Pham BT. National rehabilitation hospital limb classification for exercise, research, and clinical trials in postpolio patients. Ann N Y Acad Sci 1995;753:343-353. 28. Flansbjer UB, Drake AM, Lexell J. Reliability of ankle dorsiflexors strength measurements in persons with late effects of polio. Isokinet Exerc Sci 2011;19:55-61. 29. Flansbjer UB, Lexell J. Reliability of knee extensor and flexor muscle strength measurements in persons with late effects of polio. J Rehabil Med 2010;42:588-592. 30. Andersen H, Jakobsen J. A comparative study of isokinetic dynamometry and manual muscle testing of ankle dorsal and plantar flexors and knee extensors and flexors. Eur Neurol 1997;37:239-242. 31. Stark T, Walker B, Phillips JK, Fejer R, Beck R. Hand-held dynamometry correlation with the gold standard isokinetic dynamometry: A systematic review. PM R 2011;3:472-479. 32. Dvir Z. Isokinetics: Muscle Testing, Interpretation, and Clinical Application. 2nd ed. New York, NY: Churchill Livingstone; 2004. 33. Lexell J, Flansbjer U-B, Broga ˚rdh C. Isokinetic assessment of muscle function: Our experience with patients afflicted with selected diseases in the nervous system. Isokinet Exerc Sci 2012; 20:267-273. 34. Rekand T, Korv J, Farbu E, et al. Lifestyle and late effects after poliomyelitis. A risk factor study of two populations. Acta Neurol Scand 2004;109:120-125. 35. Werhagen L, Borg K. Analysis of long-standing nociceptive and neuropathic pain in patients with post-polio syndrome. J Neurol 2010;257:1027-1031. 36. Winberg C, Flansbjer U-B, Carlsson G, Rimmer J, Lexell J. Physical activity in persons with late effects of polio: A descriptive study. Disabil Health J 2014;7:302-308. 37. Lexell J. Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci 1995:11-16. 50 Spec No.
Disclosure U.-B.F. Department of Health Sciences, Lund University, Rehabilitation Medicine Research Group, Box 157, SE221 00 Lund, Sweden. Address correspondence to: U.-B.F.; e-mail: [email protected] Disclosures related to this publication: grant, various public and private research grant agencies and foundations (money to institution) Disclosures outside this publication: employment, Lund University; grants/ grants pending, various public and private research grant agencies and foundations (money to institution) C.B. Department of Health Sciences, Lund University, Rehabilitation Medicine Research Group, Box 157, SE221 00 Lund, Sweden; Department of Neurology and Rehabilitation Medicine, Ska ˚ne University Hospital, Lund, Sweden Disclosures related to this publication: research grant, Ska ˚ne County Council’s Research and Development Foundation (money to institution) Disclosures outside this publication: consultancy, lectures for various Swedish health authorities (money to institution); employment, Ska ˚ne University Hospital and Lund University; grants/grants pending, various public and private research grant agencies and foundations (money to institution) V.H. Department of Health Sciences, Lund University, Rehabilitation Medicine Research Group, Box 157, SE221 00 Lund, Sweden Disclosures related to this publication: grant, various public and private research grant agencies and foundations (money to institution) Disclosures outside this publication: employment, Lund University
J.L. Department of Health Sciences, Lund University, Rehabilitation Medicine Research Group, Box 157, SE221 00 Lund, Sweden; Department of Neurology and Rehabilitation Medicine, Ska ˚ne University Hospital, Lund, Sweden Disclosures related to this publication: research grant, Ska ˚ne County Council’s Research and Development Foundation (money to institution) Disclosures outside this publication: lectures and consultancies on rehabilitation methodology for various Swedish health authorities (money to institution); employment, Ska ˚ne University Hospital and Lund University; grants/grants pending, various public and private research grant agencies and foundations (money to institution); payment for lectures including service on speakers bureaus, Astra-Tech lectures; royalties, Swedish rehabilitation medicine book; travel/accommodations/meeting expenses unrelated to activities listed, CARF Surveyor reimbursement This study was accomplished within the context of the Centre of Ageing and Supportive Environments (CASE), Lund University, funded by the Swedish Council on Social Science and Working Life. Financial support was also received from ¨ sterlunds Stiftelse, Stiftelsen fo ¨r bista ˚nd a ˚t ro ¨relsehindrade i Ska ˚ne, the Alfred O and Skane County Council’s Research and Development Foundation Submitted for publication December 23, 2014; accepted May 1, 2015.
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Original Research
Men With Late Effects of Polio Decline More Than Women in Lower Limb Muscle Strength: A 4-Year Longitudinal Study ˚rdh, PT, PhD, Vibeke Horstmann, Sc lic, Ulla-Britt Flansbjer, PT, PhD, Christina Broga Jan Lexell, MD, PhD
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for one study that reported a larger and more progressive decline (5%-8% per year) [21]. Very few studies have assessed prognostic factors for the decline in muscle strength in persons with late effects of polio. One study showed that men declined more rapidly in isokinetic knee extensor strength than did women [11]. Wille ´n et al [23] found that the decline in muscle strength over 4 years was higher in persons who were stronger at the baseline assessment. In a recent study, Bickerstaffe et al [20] showed that persons with higher isometric maximal voluntary contraction (MVC) at baseline had a greater decline in strength over 10 years. Even though previous studies have evaluated the decline in muscle strength over time in persons with late effects of polio, they differ with regard to study design and the statistical methods used. To analyze longitudinal data in order to identify potential determinants, the mixed-random and fixed effect regression models (mixed linear models; MLM) are recommended [24-26]. To our knowledge, no study has used the MLM model to assess changes in muscle strength over time in persons with late effects of polio. The main aim of this study was to assess changes in strength in the knee extensor and flexor muscles and ankle dorsiflexor muscles annually over 4 years in persons with late effects of polio. The second aim was to identify determinants of changes in muscle strength, such as gender, age, age at acute polio infection, length of time with new symptoms, body mass index (BMI), and estimated baseline weakness. Methods Participants Fifty-two community-dwelling ambulant persons were recruited from a postpolio rehabilitation clinic at a university hospital in the south of Sweden. Inclusion criteria were (1) 50-75 years of age; (2) a confirmed history of acute poliomyelitis affecting the lower limbs, with new weakness after a period of functional stability of at least 15 years; and (3) ability to walk at least 300 m with or without an assistive and/or orthotic device. Exclusion criteria were (1) using a wheelchair as the main mode of transportation and (2) ongoing major depression, systemic disease, or any other disease that could affect muscle strength. The treating physician selected participants who met the inclusion and exclusion criteria and were mildly to moderately affected in their lower limbs. These persons were invited consecutively to participate in the study in connection with their regular follow-up visits to the clinic. We aimed for at least 50 participants to obtain a reasonably large sample that could be assessed annually over the 4-year period. Inclusion continued for 18 months (2007 to 2009) until 52 persons had agreed to participate.
For all 52 participants, an electromyogram had been recorded in the lower limbs (vastus lateralis and tibialis anterior muscles) as part of the initial routine clinical examination and verification of prior polio, and there were no other diseases that could explain their new symptoms. According to the National Rehabilitation Hospital (NRH) Post-Polio Limb Classification [27], all participants had postpolio NRH class II to V (indicating clinically stable or unstable polio) in at least one of their knee or ankle dorsiflexor muscles. According to each person’s own perception of his or her muscle weakness, one lower limb was defined as the “more-affected limb” and the other lower limb that was less affected or not affected was defined as the “less-affected limb.” Prior to inclusion in the study, information about the purpose of the study was provided, and each individual gave his or her written informed consent to participate. The study followed the principles of the Helsinki declaration. Muscle Strength Measurements Isokinetic concentric knee extension, knee flexion, and ankle dorsiflexion muscle strength and isometric knee extension and ankle dorsiflexion muscle strength were measured with a Biodex Multi-Joint System 3 PRO dynamometer (Biodex Medical Systems, Shirley, NY) using a standard protocol developed in our research group [28,29]. These studies have shown that lower limb muscle strength can be reliably measured in persons with late effects of polio (for knee extensors and flexors, intraclass correlation coefficients [ICC2,1] ranging from 0.85-0.99 and standard error of measurement [SEM] from 10.2-13.9 Newton meter [Nm], and for ankle dorsiflexors, ICC2,1 ranging from 0.85-0.99 and SEM from 2.5-3.7 Nm). Before each strength measurement, the range of motion was set and the Biodex software applied the gravity correction. For the knee muscle strength measurements, the participants were seated in the adjustable chair of the dynamometer without shoes or an orthotic device and were stabilized with straps across the shoulders, waist, and thigh. After a structured warm-up the participants performed 3 maximal isokinetic extensor and flexor contractions at 60 /s, and the highest peak torques were recorded (in Nm). After a 2-minute rest, the participants performed 2 maximal isometric knee extensor muscle contractions with a knee flexion angle at 90 , and the highest MVC was recorded (in Nm). For the ankle dorsiflexor strength measurements, the participants were seated in the adjustable chair of the dynamometer, with the leg elevated by a support arm just above the knee with the angles of the hip at 90 flexion and the knee joints at 30 flexion. The ankle was placed and secured on the Biodex footplate. To warm up and become familiar with the ankle dorsiflexor strength measurements, 3-5 submaximal contractions with the dorsiflexor muscles were performed. After a 1-minute
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rest, 3 maximal contractions at 30 /s were performed, with 30 seconds rest between each contraction. Each contraction started from a relaxed plantar-flexed position without any preload, and the highest peak torques were recorded (in Nm). After a 2-minute rest, testing continued with 2 maximal isometric contractions with a 60-second rest between each contraction. The ankle was fixed in 10 plantar-flexed position, and the highest MVC was recorded (in Nm). Procedures All strength measurements were performed by the same physiotherapist (U-BF). The participants were tested annually over 4 years (a total of 5 times) and as close as possible to 1 year between each test. The knee muscle strength was measured before the ankle dorsiflexor muscle strength, and the strength of the less-affected lower limb was measured before that of the more-affected lower limb. Consistent verbal encouragement was given throughout the tests. The total time for the strength measurements at each test session was approximately 1 hour. After completion of the annual test sessions, a summary of the test results was given to the participants. Statistics Data from the muscle strength measurements provided 10 quantitative variables for the analyses: 4 knee extension and 2 knee flexion strength measurements and 4 ankle dorsiflexor strength measurements. Of the 52 participants, 1 participant missed 1 test session the third year and another 3 participants missed the last 2 or 3 test sessions. The missing values were compensated for in the statistical model. Because of weakness and/or stiffness, 30 participants were unable to perform the ankle dorsiflexor strength measurements with the more-affected lower limb, and 6 participants were unable to do so with the less-affected lower limb. The statistical analyses for the ankle dorsiflexors were therefore based on 22 participants for the moreaffected lower limb and on 46 participants for the less-affected lower limb. The characteristics of the sample were described by frequencies, means, and standard deviations (SDs). Differences between men and women at baseline were analyzed by independent samples t-tests. For each participant, the predicted muscle strength for isometric knee extension and ankle dorsiflexion was calculated based on gender, age, height, and body mass specific values for a healthy population [14]. These values were used to calculate the predicted muscle weakness at baseline (ie, the differences between the predicted and the measured muscle strength values). MLM [26] were used for the longitudinal data analyses. Estimated means and SDs of all muscle strength measurements were obtained based on the covariance
3
matrix. The fixed linear effects (mean values for the group), the random effects (individual variations around the mean) and the deviations from the linear slopes over the 4 years were calculated for men and women, respectively. To analyze prognostic determinants for any changes in muscle strength, the independent variables (covariates) gender, age, age at acute polio, length of time with new symptoms, BMI, and the predicted baseline weakness in isometric muscle strength were analyzed in the mixed linear regression models. First, all covariates and their interaction with time were inserted into the models. The nonsignificant predictors were then removed in a backward manner, starting with the least significant interaction term; no covariate was removed when the interaction term was statistically significant. The final models contained only covariates where the covariate itself or its interaction with time was significant. All interval scaled variables used in the analyzes were centered to the mean, giving positive covariate values for the participants above the mean values of age, age at acute polio, time with new symptoms, BMI, and baseline weakness. The gender variable was coded 0 (women) and 1 (men). All calculations were performed using SPSS statistics software version 21.0 (IBM Corp, Armonk, NY). The significance of random effects was tested with the deviance test (2 degrees of freedom [df]) based on restricted maximum likelihood. Significance levels below .05 represent statistical significance. Results In Table 1, the characteristics of the 52 participants (28 men and 24 women) are presented. Their mean age at the study enrollment was 64 years (SD 6, range 5274), and the mean time since onset of new symptoms was 13 years (SD 7, range 2-28). Fifty-two percent were most affected in their right lower limb, and 71% had verified prior polio in both lower limbs. Walking aids were used by 10% of the participants and ankle foot orthoses were used by 19%. The mean time between each test session was close to 1 year (12.1 months, SD 0.8), and the participants were all free from acute illnesses and injuries at each testing session. At baseline the men were significantly stronger than the women in all knee muscle strength measurements and for the less-affected lower limb regarding ankle dorsiflexor strength, and thus data for the men and women were analyzed separately. Linear Trends and Random Effects in Muscle Strength Over Time In Tables 2 and 3, time from baseline and the estimated means and SDs at each test occasion over the
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Muscle Strength and Late Effects of Polio
The men experienced a significant fixed linear decline over time for all knee muscle strength measurements, ranging from 1.0 to 4.5 Nm/y (from 1.4% [P <.05] per year for the less-affected isokinetic knee flexion to 4.2% [P < .001] for more-affected isokinetic knee extension; Table 2). For the ankle dorsiflexors, a significant fixed linear effect of time was found only for isokinetic muscle strength in the more-affected limb and for isometric muscle strength in the less-affected limb, ranging from 0.82 to 0.42 Nm/y, respectively (3.3%-1.4% per year [P < .05]). The random effect of time was significant for all strength measurements of the less-affected limb, as well as for isokinetic measurements of the more-affected limb (deviance [df ¼ 2]: 7.7 (P < .05) to 14.6 [P < .01]). For the women (Table 3), no significant fixed linear decline over time was observed for the knee muscle strength measurements. There was a significantly increased isometric ankle dorsiflexor muscle strength (P < .01) for both the less-affected lower limbs (0.71 Nm/y; 4.0%) and the more-affected lower limbs (0.87 Nm/y; 5.5%), but no significant fixed linear effect of time for isokinetic ankle dorsiflexor strength measurements. A significant random effect of time was found for 3 of the strength measurements in the lessaffected limb (isokinetic knee extensors and isokinetic and isometric ankle dorsiflexors; deviance [df ¼ 2] 7.8 [P < .05] to 13.3 [P < .01]), but no significant random effect was found for the more-affected limb. Over the 4 years, no significant deviation from the linear slopes occurred for any strength measurement, either for the men or for the women, indicating that the change in muscle strength over time did not accelerate.
Table 1 Characteristics of the 52 participants with late effects of polio Characteristic
Values
Gender Men Women Age, y BMI Age at acute polio infection, y Time with new symptoms, y Most-affected leg Right Left Both lower limbs affected by polio Walking aid None Stick or crutch Rollator Orthotic device None Ankle-foot orthosis Baseline isometric weakness, Nm* Less-affected knee extension More-affected knee extension Less-affected ankle dorsiflexors More-affected ankle dorsiflexors
28 24 64 26 5 13
(54) (46) (6); 52-74 (3); 21-37 (4); 0-15 (7); 2-28
27 (52) 25 (48) 37 (71) 47 (90) 4 (8) 1 (2) 42 (81) 10 (19) 66 115 18 11
(50); (51); (12); (10);
40-250 40-251 3-39 10-43
Values are represented as n (%) or mean (SD); range. SD ¼ standard deviation; BMI ¼ body mass index; Nm ¼ Newton meter. * For each participant the baseline isometric weakness was calculated as the difference between the predicted muscle strength based on age, gender, length, and body weight specific values for a healthy population [14] and the measured muscle strength value.
4 years, along with the fixed linear effects for the group and the random effects for the individuals, are presented for men and women, respectively.
Table 2 Estimated mean of strength measurements for knee extensors, knee flexors, and ankle dorsiflexors (Newton meter) in 28 men with late effects of polio Estimated Mean of Fixed Effects Test Assessment Less-affected lower limb Knee extensors isokinetic 60 /s Knee flexors isokinetic 60 /s Knee extensors isometric MVC Ankle dorsiflexors isokinetic 30 /s§ Ankle dorsiflexors isometric MVC§ More-affected lower limb Knee extensors isokinetic 60 /s Knee flexors isokinetic 60 /s Knee extensors isometric MVC Ankle dorsiflexors isokinetic 30 /s{ Ankle dorsiflexors isometric MVC{
Baseline
After 1 y
After 2 y
After 3 y
After 4 y
Fixed Linear Effect
Random Effect†
130.1 71.0 158.4 28.8 30.6
(9.0) (5.0) (10.6) (2.2) (2.7)
130.6 73.4 155.0 28.6 30.0
(9.0) (5.0) (10.6) (2.2) (2.7)
124.4 70.8 147.4 28.0 30.8
(9.1) (5.0) (10.6) (2.2) (2.7)
123.4 67.7 140.7 28.7 31.4
(9.1) (5.0) (10.6) (2.2) (2.7)
122.2 68.7 143.3 28.4 32.1
(9.1) (5.0) (10.6) (2.2) (2.7)
2.30** 1.00* 4.47*** 0.06‡ 0.42
9.8** 12.7** 8.4* 10.2** 14.6**
91.0 51.0 96.3 24.6 24.0
(9.2) (4.8) (10.7) (3.3) (4.0)
91.3 52.3 95.6 26.3 23.9
(9.2) (4.8) (10.7) (3.3) (4.0)
84.4 49.7 93.6 23.9 23.6
(9.2) (4.8) (10.7) (3.3) (4.0)
81.7 46.8 86.1 22.6 22.8
(9.3) (4.9) (10.7) (3.3) (4.0)
76.5 48.3 86.6 22.3 23.6
(9.3) (4.9) (10.7) (3.3) (4.0)
3.83*** 1.07* 2.85*** 0.82* 0.18‡
8.6* 7.7* 1.06‡ 12.6** 1.9‡
Estimated values are presented as mean (SD). SD ¼ standard deviation; MVC ¼ maximal voluntary contraction. *P < .05. **P < .01. ***P < .001. † Deviance (df ¼ 2). ‡ Not significant. § Participants able to perform the measurements: n ¼ 24. { Participants able to perform the measurements: n ¼ 12. FLA 5.2.0 DTD PMRJ1488_proof 27 May 2015 11:55 am ce
561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616 617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640
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721 722 723 Estimated Mean of Fixed Effects 724 725 Baseline After 1 y After 2 y After 3 y After 4 y Test Assessment Fixed Linear Effect Random Effect† 726 727 Less-affected lower limb 728 Knee extensors isokinetic 60 /s 81.8 (6.1) 80.8 (6.1) 77.9 (6.1) 80.7 (6.1) 80.9 (6.1) 0.19‡ 7.8* 729 Knee flexors isokinetic 60 /s 40.3 (3.0) 42.7 (3.0) 42.1 (3.0) 41.4 (3.0) 44.4 (3.0) 0.68‡ 2.4‡ 730 ‡ ‡ Knee extensors isometric MVC 92.9 (6.9) 86.0 (6.9) 86.1 (6.9) 85.2 (6.9) 86.4 (6.9) 1.38 5.8 731 Ankle dorsiflexors isokinetic 30 /s§ 19.5 (1.4) 20.2 (1.4) 20.3 (1.4) 19.7 (1.4) 19.6 (1.4) 0.04‡ 13.3** 732 733 Ankle dorsiflexors isometric MVC§ 17.7 (1.6) 18.1 (1.6) 18.8 (1.6) 19.5 (1.6) 20.6 (1.6) 0.71** 9.5** 734 More-affected lower limb 735 Knee extensors isokinetic 60 /s 59.0 (6.2) 61.9 (6.2) 58.9 (6.2) 58.4 (6.2) 58.7 (6.2) 0.43‡ 1.1‡ 736 ‡ ‡ Knee flexors isokinetic 60 /s 25.4 (2.9) 26.0 (2.9) 26.2 (2.9) 26.0 (2.9) 27.8 (2.8) 0.47 1.7 737 Knee extensors isometric MVC 61.0 (6.8) 62.7 (6.8) 61.7 (6.8) 60.1 (6.8) 60.8 (6.8) 0.30‡ 0.7‡ 738 739 Ankle dorsiflexors isokinetic 30 /s{ 16.8 (2.5) 16.8 (2.5) 17.5 (2.5) 17.3 (2.5) 17.0 (2.5) 0.10‡ 3.9‡ 740 Ankle dorsiflexors isometric MVC{ 15.9 (2.4) 19.1 (2.4) 17.2 (2.4) 20.4 (2.4) 19.6 (2.4) 0.87** 2.8‡ 741 Estimated values are presented as mean (SD). 742 743 SD ¼ standard deviation; MVC ¼ maximal voluntary contraction. 744 *P < .05. 745 **P < .01. 746 Q3 ***P < .001. 747 † Deviance (df ¼ 2). 748 ‡ 749 Not significant. § 750 Participants able to perform the measurements: n ¼ 22. { 751 Participants able to perform the measurements: n ¼ 10. 752 753 754 Discussion Determinants of Change in Muscle Strength Over 755 756 Time 757 This longitudinal study over 4 years found that men 758 759 with late effects of polio declined more in muscle All covariates and interactions with time that were 760 strength than did women. Men had a significant effect significantly related to knee muscle strength are pre761 over time for all knee muscle strength measurements sented as the final model in Table 4. The strongest in762 763 and for 2 of the ankle dorsiflexors muscle strength fluence was found for the participants’ gender; the 764 measurements (P < .05 to P < .001). Women had a sigdecline in strength over time was significantly larger for 765 766 nificant effect only for the isometric ankle dorsiflexor the men than for the women for all knee muscle 767 strength measurements. No significant deviations from strength measurements in the more-affected lower limb 768 the linear slopes occurred over the 4 years. The stronand for the knee flexor strength in the less-affected 769 770 gest prognostic determinant for the decline in muscle lower limb. Among the other covariates, the only 771 strength was the participants’ gender. interaction with time was found for the more affected 772 773 Several factors may explain the differences between isokinetic knee extensor strength measurements. 774 the results in the present and previous studies. In the Younger persons, those who have had new symptoms for 775 776 present study, we found a decline in knee muscle a longer time, and those with less baseline weakness 777 strength measurements for men (4.5% and 1.8% per declined more in muscle strength, even though the in778 year) but no significant linear trend for any of the knee teractions with time were quite small. 779 780 muscle strength measurements for women. Instead, we All covariates and the interactions with time that 781 found a significant positive linear trend for isometric were significantly related to ankle dorsiflexor muscle 782 783 ankle dorsiflexor strength measurements. Contrary to strength are presented as the final model in Table 5. 784 previous studies [11,20,21,23], our population consisted The strongest influence was found for the participants’ 785 of roughly equal proportions of men and women (54% gender; the men were significantly stronger at baseline 786 787 men). The balanced gender distribution made it possible in both the less- and more-affected lower limb. The 788 for us to analyze if there were any differences for the men only interaction with time was for isokinetic dorsi789 790 and the women in muscle strength over 4 years. In other flexion in the more-affected lower limb; the decline in 791 studies [20,21,23] the measurements for men and women muscle strength was significantly larger for the men 792 were combined, and only one study has shown that men than for the women. For all other covariates, there 793 794 decline more rapidly in muscle strength than women with were only 2 minor interactions with time in the more 795 regard to isokinetic knee extension strength [11]. affected ankle dorsiflexor measurements, namely, 796 797 The characteristics of the participants could also those with more baseline weakness and older persons. 798 have influenced the results. Many studies of persons These participants had declined more in muscle 799 800 with late effects of polio were published between 1994 strength over time.
Table 3 Estimated mean of strength measurements for knee extensors, knee flexors and ankle dorsiflexors (Newton meter) in 24 women with late effects of polio
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801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821 822 823 824 825 826 827 828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843 844 845 846 847 848 849 850 851 852 853 854 855 856 857 858 859 860 861 862 863 864 865 866 867 868 869 870 871 872 873 874 875 876 877 878 879 880
6
Table 4 Knee muscle strength measurements and the final models with covariates and interaction with time for the total sample
Less-affected lower limb Isokinetic extensors Isokinetic flexors Isometric MVC extensors More-affected lower limb Isokinetic extensors Isokinetic flexors Isometric MVC extensors
Age‡
Age *Time
BMI
BMI *Time
Age Acute Polio
Age Acute Polio *Time
Intercept
Trend
Gender†
Gender *Time
80.0 39.2 90.5
1.3§ 0.7§ 3.0**
54.1*** 35.4*** 72.7***
e 1.8* e
1.5* 1.1* e
e e e
e e 2.0*
e e e
2.3* 2.2** e
e e e
42.0 18.4 41.5
0.6§ 0.5§ 0.3§
69.6*** 40.2*** 76.5***
4.9*** 1.6* 2.6*
1.4* 0.9* 1.2*
0.2* e e
e e 2.4*
e e e
e 1.4* e
e e e
PPS
PPS *Time
Less Aff Weakness
Less Aff Weakness *Time
More Aff Weakness
More Aff Weakness *Time
e e
e e
0.6*** 0.2*** 0.8***
e e e
e e e
e e e
0.2§ e e
0.2* e e
0.1* 0.1** 0.2**
e e e
0.9*** 0.3*** 1.0***
0.03* e e
Table 5 Ankle dorsiflexor muscle strength measurements and the final models with covariates and interaction with time for the total sample
Age‡
Age *Time
Age Acute Polio
Age Acute Polio *Time
BMI
BMI *Time
PPS
PPS *Time
Less Aff Weakness
Less Aff Weakness *Time
More Aff Weakness
More Aff Weakness *Time
Intercept
Trend
Gender†
Gender *Time
19.4 16.1
0.1§ 0.5**
9.9*** 14.3***
e e
e e
e e
e e
e e
e e
e e
e e
e e
0.7*** 0.9***
e e
e e
e e
14.2 12.3
0.6§ 0.1§
13.5*** 14.7***
1.4** e
e 0.2§
e 0.1*
e
e
e e
e e
e e
e e
e e
e e
0.8*** 0.9***
0.1** e
{
Less-affected lower limb Isokinetic strength Isometric MVC More-affected lower limb# Isokinetic strength Isometric MVC
Intercept and trend for the significant factors in the final model for each strength measurement. BMI ¼ body mass index; PPS ¼ time with late effects of polio; less aff weakness ¼ baseline weakness for less-affected isometric knee extensor muscle strength; more aff weakness ¼ baseline weakness for more-affected isometric knee extensor muscle strength; MVC ¼ maximal voluntary contraction. *P < .05. **P < .01. ***P < .001. † Woman is reference category. ‡ Baseline age. § Not significant. { Participants able to perform the measurements: n ¼ 46. # Participants able to perform the measurements: n ¼ 22.
Muscle Strength and Late Effects of Polio
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Intercept and trend for the significant factors in the final model for each strength measurement. BMI ¼ body mass index; PPS ¼ time with late effects of polio; less aff weakness ¼ baseline weakness for less-affected isometric knee extensor muscle strength; more aff weakness ¼ baseline weakness for more-affected isometric knee extensor muscle strength; MVC ¼ maximal voluntary contraction. *P < .05. **P < .01. ***P < .001. † Woman is reference category ‡ Baseline age. § Not significant.
881 882 883 884 885 886 887 888 889 890 891 892 893 894 895 896 897 898 899 900 901 902 903 904 905 906 907 908 909 910 911 912 913 914 915 916 917 918 919 920 921 922 923 924 925 926 927 928 929 930 931 932 933 934 935 936 937 938 939 940 941 942 943 944 945 946 947 948 949 950 951 952 953 954 955 956 957 958 959 960
961 962 963 964 965 966 967 968 969 970 971 972 973 974 975 976 977 978 979 980 981 982 983 984 985 986 987 988 989 990 991 992 993 994 995 996 997 998 999 1000 1001 1002 1003 1004 1005 1006 1007 1008 1009 1010 1011 1012 1013 1014 1015 1016 1017 1018 1019 1020 1021 1022 1023 1024 1025 1026 1027 1028 1029 1030 1031 1032 1033 1034 1035 1036 1037 1038 1039 1040
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and 1998 [11,16-19]. In the present study the participants were generally older (mean age 64 years) compared with other studies, where the mean age was around 50 years [11,16-18,20,21]. Even if the participants in this study were older, no deviations from the linear slopes occurred over the 4 years, and age explained only a small additional part of the linear trend. Thus, it seems that the decline in muscle strength in older persons with late effects of polio is fairly stable. Furthermore, in previous studies, isometric knee extension strength has been the most common measurement, and the values at baseline have varied between 57 and 176 Nm [11,16,18,20]. In many studies only one limb has been measured [16-18,20], so the isometric knee extension muscle strength can be a measure of either the more or the less affected lower limb, and therefore the strength values are not comparable with those of our study. Another factor that might have influenced the results is the outcome measurement used. To be able to follow muscle strength over time, reproducible and sensitive measurement tools are needed. For many years manual muscle testing and a handheld dynamometer have been used to measure muscle strength in persons with late effects of polio. However, these measurements are less reproducible and sensitive than isokinetic dynamometry [30,31]. In this study we used isokinetic dynamometry, which is currently the recommended measurement tool to evaluate changes in muscle strength over time [32,33]. Furthermore, the test protocols were standardized and carefully followed at each test session. Other factors that could have influenced the result are the frequency of strength measurements and the length of follow-ups. In our study, all participants were measured annually over 4 years, the minimum follow-up time suggested for persons with late effects of polio [15]. In most previous studies the follow-up times have varied between 4 and 10 years [16-18,20,21,23], but only 2 studies have performed the measurements annually [18,21]. If the follow-up time is short, long-term changes are difficult to estimate; on the other hand, if annual measurements are performed, a progressive decline in muscle strength can more easily be detected. In one study with annual follow-ups, including 23 persons with late effects of polio (stable and unstable; ie, those with new weakness) and 14 healthy control subjects [18], no significant differences in the mean change in muscle strength (the slope of the lines) for the 3 groups were found over a 7-year period. In the other study [21], a large decline in strength occurred over 5 years. Isokinetic knee muscle strength at 60 /s declined 7.8% for the extensors and 5.1% for the flexors per year with a progressive decline in strength over time. However, the progressive decline was not significant, probably because of a large number of dropouts; only 8 of the 76 baseline limb measurements were repeated during the entire period. In our study, almost all participants
7
performed every test session, and no significant change of the slope over time was found, indicating that the change in muscle strength was similar over time. The statistical method used also could have influenced the results. We used the MLM models, which are recommended for longitudinal clinical studies [24-26]. The MLM technique takes into account the correlation between the measures obtained in the same persons, as well as missing observations. The MLM combines the effect of average time with any individual variation over time (linear trends, random effects, and changes in the slope). To be able to calculate deviations from the linear slopes over time, at least 3 measurement points are required [25]. In previous follow-up studies in persons with late effects of polio, older and more traditional statistical methods have been used to analyze the longitudinal data, and most participants have only been measured twice. To our knowledge, this study is the first using the MLM in a longitudinal study of the annual decline in muscle strength in persons with late effect of polio. Few studies [11,20,23] have analyzed potential prognostic factors for a change in muscle strength. In this study, we formed a model with covariates and identified different significant factors that could explain parts of the outcome for the strength measurements. The covariatesdgender, age, and BMIdwere chosen because they are of importance when calculating normal values for muscle strength [14]. The final model showed that gender was the strongest predictor for the effect of time and only for isokinetic knee extensors in the more affected lower limb; baseline weakness together with age and time with new symptoms could explain a small additional part of the linear trend. In a study by Wille ´n et al [23], the decrease in muscle strength was higher in persons who were stronger at the baseline assessment for both isokinetic knee flexion and ankle dorsiflexion. In another study, men declined more rapidly in knee extensor strength than did women, but only for isokinetic strength [11]. Taken together, more studies are needed to control for the effect of gender. There might be other factors not used in our model with covariates, such as pain, fatigue, physical activity, or the size of motor units at baseline, that could explain the differences between men and women [4,34-36] . Strengths and Limitations Only 4 persons missed 1 to 3 test sessions during the 4 years (altogether, 8 out of a total of 260), which could be considered a very low dropout rate, especially because the statistical model compensated for the missing values. Both lower limbs were measured and the less affected limbs in 15 participants were “almost” healthy because they did not have any polio-related weakness in that limb. Even though persons with late effects of polio are a heterogeneous group, the paresis in the lower limb can differ within the limb, as well as between limbs. In addition, the weakness in one lower
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Muscle Strength and Late Effects of Polio
limb has probably had an influence on the other limb during mobility-related activities since childhood. In this study, we measured knee muscle strength and ankle dorsiflexor strength. Strength measurements in these muscles have been shown to be reproducible using a Biodex dynamometer [28,29]. Other muscle groups, such as the hip extensors and flexors, could have been selected because they are also related to gait performance. However, our clinical experience is that they are less affected in persons with late effect of polio and therefore they were not measured. Furthermore, these muscles are more difficult to measure isokinetically than knee extensors, knee flexors, and ankle dorsiflexors, and no data are available on the reproducibility of isokinetic measurements of these muscles in persons with late effects of polio. For ankle muscle strength measurements, the variation over time was hardly significant. However, few participants (n ¼ 22) could perform measurement of their more-affected ankle dorsiflexors; several participants had a pronounced weakness in this muscle group and were therefore unable to perform any active movement in the ankle. On the other hand, 46 of the participants were able to perform the ankle dorsiflexor measurements in the less-affected lower limb, and there were no discernible differences between the more-affected and the lessaffected lower limb. The positive linear trends for the ankle dorsiflexor muscles for both men and women are somewhat surprising but could be due to the fact that we had a selected group of participants or due to a learning effect. A small nonsignificant learning effect has been reported in a previous test-retest reliability study [28], and the technique to perform the measurements might be improved when repeated several times. In future research other measurement modes, such as passive modes, might be more useful in very weak muscles. Overall, we found small changes in muscle strength over time, which could be due to both the study sample and the length of follow-up. Not enough data are available to perform a comprehensive power analysis, because gender differences have not been the primary aim of previous studies of changes in muscle strength in persons with late effect of polio. A sample size of 52 persons could be considered small, but annual data collection is very time consuming for both participants and assessors. It is important that the assessments be performed regularly and by the same assessor following a strict protocol. We chose to follow up the participants for 4 years because this period has been recommended as the minimum follow-up time for persons with late effects of polio [15]. Compared with previous studies with annual measurements [18,21], and taking into account the very low dropout rate in this study, we still believe the number of participants to be satisfactory for this type of analysis. All participants were ambulant and had mild to moderate late effects of polio. They were weaker in the ankle dorsiflexors than in their knee muscles, and this weakness
was compensated for by an ankle-foot orthosis in 10 participants, but no one needed a knee-ankle-foot orthosis. Thus the results in this study are limited to persons with mild to moderate disability. In future studies a larger sample with a wider range of disability, as well as a longer follow-up period, would be desirable. However, some of the participants in this study were already quite old (at the last test session the oldest person was 78 years), and a reduction in muscle strength will probably continue in both men and women as a result of normal aging [37]. Conclusion Small changes in muscle strength were seen in persons with late effects of polio over 4 years. The strongest predictor of change in lower limb muscle strength was the participants’ gender. Men declined more in muscle strength than did women, especially in the knee muscles, but the rate of the decline did not accelerate over time, which indicates that gender could be a contributing factor to the progressive decline in muscle strength in persons with late effects of polio. References 1. Farbu E, Gilhus NE, Barnes MP, et al. EFNS guideline on diagnosis and management of post-polio syndrome. Report of an EFNS task force. Eur J Neurol 2006;13:795-801. 2. Trojan DA, Cashman NR. Post-poliomyelitis syndrome. Muscle Nerve 2005;31:6-19. 3. Halstead LS, Rossi CD. New problems in old polio patients: Results of a survey of 539 polio survivors. Orthopedics 1985;8:845-850. 4. Jensen MP, Alschuler KN, Smith AE, Verrall AM, Goetz MC, Molton IR. Pain and fatigue in persons with postpolio syndrome: Independent effects on functioning. Arch Phys Med Rehabil 2011; 92:1796-1801. 5. Boyer FC, Tiffreau V, Rapin A, et al. Post-polio syndrome: Pathophysiological hypotheses, diagnosis criteria, drug therapy. Ann Phys Rehabil Med 2010;53:34-41. 6. Lexell J, Broga ˚rdh C. Life satisfaction and self-reported impairments in persons with late effects of polio. Ann Phys Rehabil Med 2012;55:577-589. 7. Broga ˚rdh C, Flansbjer UB, Espelund C, Lexell J. Relationship between self-reported walking ability and objectively assessed gait performance in persons with late effects of polio. NeuroRehabilitation 2013;33:127-132. 8. Horemans HL, Bussmann JB, Beelen A, Stam HJ, Nollet F. Walking in postpoliomyelitis syndrome: The relationships between timescored tests, walking in daily life and perceived mobility problems. J Rehabil Med 2005;37:142-146. 9. Wille ´n C, Sunnerhagen KS, Ekman C, Grimby G. How is walking speed related to muscle strength? A study of healthy persons and persons with late effects of polio. Arch Phys Med Rehabil 2004;85: 1923-1928. 10. Laffont I, Julia M, Tiffreau V, Yelnik A, Herisson C, Pelissier J. Aging and sequelae of poliomyelitis. Ann Phys Rehabil Med 2010;53:24-33. 11. Agre JC, Grimby G, Rodriquez AA, Einarsson G, Swiggum ER, Franke TM. A comparison of symptoms between Swedish and American post-polio individuals and assessment of lower limb strengthda four-year cohort study. Scand J Rehabil Med 1995;27: 183-192. 12. Bartels MN, Omura A. Aging in polio. Phys Med Rehabil Clin N Am 2005;16:197-218.
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Disclosure U.-B.F. Department of Health Sciences, Lund University, Rehabilitation Medicine Research Group, Box 157, SE221 00 Lund, Sweden. Address correspondence to: U.-B.F.; e-mail: [email protected] Disclosures related to this publication: grant, various public and private research grant agencies and foundations (money to institution) Disclosures outside this publication: employment, Lund University; grants/ grants pending, various public and private research grant agencies and foundations (money to institution) C.B. Department of Health Sciences, Lund University, Rehabilitation Medicine Research Group, Box 157, SE221 00 Lund, Sweden; Department of Neurology and Rehabilitation Medicine, Ska ˚ne University Hospital, Lund, Sweden Disclosures related to this publication: research grant, Ska ˚ne County Council’s Research and Development Foundation (money to institution) Disclosures outside this publication: consultancy, lectures for various Swedish health authorities (money to institution); employment, Ska ˚ne University Hospital and Lund University; grants/grants pending, various public and private research grant agencies and foundations (money to institution) V.H. Department of Health Sciences, Lund University, Rehabilitation Medicine Research Group, Box 157, SE221 00 Lund, Sweden Disclosures related to this publication: grant, various public and private research grant agencies and foundations (money to institution) Disclosures outside this publication: employment, Lund University
J.L. Department of Health Sciences, Lund University, Rehabilitation Medicine Research Group, Box 157, SE221 00 Lund, Sweden; Department of Neurology and Rehabilitation Medicine, Ska ˚ne University Hospital, Lund, Sweden Disclosures related to this publication: research grant, Ska ˚ne County Council’s Research and Development Foundation (money to institution) Disclosures outside this publication: lectures and consultancies on rehabilitation methodology for various Swedish health authorities (money to institution); employment, Ska ˚ne University Hospital and Lund University; grants/grants pending, various public and private research grant agencies and foundations (money to institution); payment for lectures including service on speakers bureaus, Astra-Tech lectures; royalties, Swedish rehabilitation medicine book; travel/accommodations/meeting expenses unrelated to activities listed, CARF Surveyor reimbursement This study was accomplished within the context of the Centre of Ageing and Supportive Environments (CASE), Lund University, funded by the Swedish Council on Social Science and Working Life. Financial support was also received from ¨ sterlunds Stiftelse, Stiftelsen fo ¨r bista ˚nd a ˚t ro ¨relsehindrade i Ska ˚ne, the Alfred O and Skane County Council’s Research and Development Foundation Submitted for publication December 23, 2014; accepted May 1, 2015.
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