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Journal of Back and Musculoskeletal Rehabilitation 29 (2016) 31–40 DOI 10.3233/BMR-150592 IOS Press

Is the Sørensen test valid to assess muscle fatigue of the trunk extensor muscles? Christophe Demoulina,b,∗, Mathieu Boyera , Jacques Duchateauc, Stéphanie Grosdenta,b , Boris Jidovtseffa, Jean-Michel Crielaarda,b and Marc Vanderthommena,b a

Department of Sport and Rehabilitation Sciences, University of Liege, Liege, Belgium Department of Physical Medicine and Rehabilitation, Liege University Hospital Center, Liege, Belgium c Laboratory of Applied Biology and Research Unit in Neurophysiology, Université Libre de Bruxelles, Brussels, Belgium b

Abstract. BACKGROUND: Very few studies have quantified the degree of fatigue characterized by the decline in the maximal voluntary contraction (MVC) force of the trunk extensors induced by the widely used Sørensen test. OBJECTIVE: Measure the degree of fatigue of the trunk extensor muscles induced by the Sørensen test. METHODS: Eighty young healthy subjects were randomly divided into a control group (CG) and an experimental group (EG), each including 50% of the two genders. The EG performed an isometric MVC of the trunk extensors (pre-fatigue test) followed by the Sørensen test, the latter being immediately followed by another MVC (post-fatigue test). The CG performed only the preand post-fatigue tests without any exertion in between. RESULTS: The comparison of the pre- and post-fatigue tests revealed a significant (P < 0.05) decrease in MVC force normalized by body mass (−13%) in the EG, whereas a small increase occurred in the CG (+2.7%, P = 0.001). CONCLUSIONS: This study shows that the Sørensen test performed until failure in a young healthy population results in a reduced ability of the trunk extensor muscles to generate maximal force, and indicates that this test is valid for the assessment of fatigue in trunk extensor muscles. Keywords: Isometric exercise, spinal muscles, fatigability, muscle endurance, low back pain

1. Introduction In 1964, Hansen developed a test for evaluating the isometric endurance of the trunk extensor muscles and validated it in 168 healthy individuals and 90 patients who had had surgery for low back pain (LBP) [1]. In this test, the subject lies in a prone position with the lower body fixed to the examining table and the upper body extending beyond the edge of the table. The test consists of holding the upper body horizontal as long as possible. Later, Biering-Sørensen used the same test together with several other evaluations with over 900 individuals and concluded that a shorter position holding time during the test was able to pre∗ Corresponding author: Christophe Demoulin, ISEPK (B21), Allée des Sports 4, B-4000 Liege, Belgium. Tel.: +32 4 366 38 97; Fax: +32 4 366 29 01; E-mail: [email protected].

dict LBP within the next year in males [2]. Since its publication in 1984, the test has become known as the “Sørensen test”. Since then, this test has been used widely [3] and is currently a common reference tool to assess muscular performance of trunk muscles in patients with LBP as well as their progress following therapeutic exercise interventions [4,5] or a rehabilitation program [6,7]. Furthermore, the Sørensen test is also frequently included in physical fitness battery tests for athletes [8,9] or the general population [10]. The clinimetric properties of the Sørensen test, which have been investigated extensively, appear generally satisfactory [3]. It has also frequently been coupled to the recording of surface electromyography (S-EMG) to obtain a deeper knowledge of muscular activities during its realization [3,11,12]. Some of these studies have concluded that the Sørensen test is not specific to back muscles as it involves the contribution of hip extensors, indicating that this test should

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be considered as a “trunk extensor test” [11,13]. The median frequency and mean power frequency of the trunk extensor muscles, and their rates of change have frequently been recorded during the test [14,15]. However, even if most of these studies report that the Sørensen test induces changes in the EMG power spectrum, this approach is only indirect and relies on physiological responses accompanying fatigue [16,17]. It is indeed not clear whether the EMG changes during a sustained task are the consequence of central fatigue or the result of neural adjustments by the central nervous system to optimize motor output, reducing thereby metabolic cost [18]. Furthermore, the EMG signal is confounded by the presence of cancellation, which refers to the loss of signal content resulting from the overlapping of positive and negative phases of the motor unit potential [19]. For these reasons, some researchers prefer to use the reduction in maximal force as a criterion to quantify the degree of muscle fatigue [20]. No well-conducted study has quantified the effect of the Sørensen test on the decline in the maximal force measured immediately after the task. Crowther et al. [21] reported that the Sørensen test did not result in a decrease in the force produced during a maximal voluntary contraction (MVC) of the trunk extensors assessed on a specific dynamometer in 20 healthy students, suggesting an absence of fatigue in these muscles. In contrast, Champagne et al. [22] reported a significant decrease in maximal static lift force after performing a modified Sørensen test in 16 elderly and 20 young male adults. Taking into account these contradictory results and the various factors limiting their interpretation, e.g. small sample size, testing positions for the MVC tests which differ from the Sørensen test, and the delay between the end of the Sørensen test and the post-MVC test (20–30 seconds in Crowther et al.’s study [21]), further investigations appear necessary. Therefore, the main aim of this study is to provide an answer to the question “Does the Sørensen test really fatigue the trunk extensor muscles?”, the term “fatigue” being quantified by the decrease in MVC force [23]. To achieve this goal, the force of the trunk extensors measured immediately after the end of the Sørensen test was compared to that of the pre-fatigue condition. Taking into account the mean holding time (two to three minutes) and the intensity of muscle contractions elicited by the Sørensen test (about 40–50% of the MVC force [3,13,24]), we expected it would result in a significant decrease in the MVC force of the trunk extensor muscles. Considering that most stud-

ies report a gender difference in performance during the Sørensen test [3,12,13,24,25], a secondary aim of this study is to compare the fatigability following the Sørensen test in both males and females.

2. Materials and methods 2.1. Experimental approach to the problem The participants took part in two sessions in laboratory settings that included a familiarization session followed by an experimental session (48–96 hours later). After the familiarization session, participants were randomized into a control group (CG) and an experimental group (EG). Males and females were separated before randomization so that both groups had a similar gender proportion. During the experimental session, both groups performed the MVC test (pre-fatigue test). Following the MVC test, the EG performed the Sørensen test as described by Demoulin et al. [26]. This was then followed, as soon as possible, by a second MVC test (post-fatigue test); the time (in second) between both tests was recorded. In contrast, the CG did not perform the Sørensen test but rested in the prone position. The duration of the resting position depended on the test holding time of the EG participants (each CG participant was matched with an EG participant) so that the duration between the test and retest was identical in both groups. This resting period was followed by the MVC test (post-test). The change in the peak force (PF) was the primary outcome. The fatigue index, expressed in percentage (%), was calculated using the formula: [1 – (post-test PF / pre-test PF)]*100 2.2. Subjects Eighty participants, aged between 18 and 25 years old (50% of females), were recruited from the students of the University of Liege by means of advertisement. The exclusion criteria included any of the following: present or past spinal or lower extremity pain that induced a limitation in functional tasks or daily living activities, previous spinal or lower extremity surgery, present or recent (< 2 years) pregnancy, medical conditions that could make physical effort unsafe (e.g. cardiac disease), and performing more than three hours of regular exercise per week.

C. Demoulin et al. / The Sørensen test is a fatiguing task

All subjects were informed of the objective of the project and took part in the study after informed consent had been obtained. The rights of human subjects were protected at all times. This study was approved by the Liege University Hospital Human Ethics Committee. 2.3. Procedures 2.3.1. Familiarization session (S1) This session started with one of the author (physiotherapist) ensuring that the participant met the eligibility criteria. Then, the participant experienced the Sørensen test and the isometric MVC test of the trunk extensors. This included the following successive steps: a) A warm-up phase, consisting of a five-minute warm-up on a bicycle (50 watts) followed by a specific exercise consisting of 30 dynamic trunk flexion-extensions in a standing position while maintaining the physiological lumbar lordosis. b) An installation phase during which the particiR ) that was used to pant wore a harness (Petzl record the MVC force. To make the system comfortable, a sponge was inserted between the chest and the harness (Fig. 1a). Then, the participant lay in a prone position on an examining table with the anterior superior iliac spines aligned with the edge of the table. Wide canvas straps secured the calves, thighs, and buttocks. The participant’s trunk rested on a block of polystyrene (perforated in the center for the ring harness), which was placed on the examination table adjusted in height so that the trunk was held in a horizontal position. A metallic chain was used to link the ring harness to a tension-compression load cell (Honeywell Sensotec Model 34, 1000 g to 1000 lb, Columbus, OH, USA) attached to the floor. The signal from the load cell was amplified (Honeywell Sensotec Inline Amp P/N 0606827-02, Columbus, OH, USA) before its recording on a computer at a sampling rate of 20 Hz. This chain was positioned vertically and adjusted in length so that it was stretched when the trunk was in the horizontal position (Fig. 1b). c) The MVC test (Fig. 1c). Before beginning the test, the subject performed four graded submaximal isometric contractions (spaced by 30 seconds of rest) of the trunk extensors (effort to lift the upper body) whereby she/he built up to a nearmaximum effort on the last repetition to be fa-

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miliarized with the MVC test. One minute after these familiarization contractions, three isometric MVCs were performed at one-minute intervals. Standardized instructions were given as follows: “I will count to three; push with increasing intensity so that your effort is at its maximum when I say ‘three.’ Then relax progressively.” For each trial, the highest instantaneous force, i.e., the peak force (PF), was expressed in Newtons (N) on the computer screen and was normalized to body weight (relative PF expressed in N·kg−1 ) to remove the influence of individual mass. The participant was given an extra trial if the third effort revealed the greatest PF; the highest relative PF was then selected. Three minutes of rest, spent in this position (with the trunk resting on the polystyrene block), were then allowed prior to performing the Sørensen test. d) The Sørensen test (Fig. 1d). Before beginning the test, the chain was detached from the harness ring and the block was removed (the participant was instructed to press his/her forearms on the table). The subject was then asked to bend his/her arms against the chest and maintain the upper body in the horizontal position while holding the head in a neutral position. The horizontality of the trunk during the test was controlled by means of a static reference (stadiometer); as soon as the contact with this was lost, the examiner asked the participant to correct the position. The test ended when the subject was no longer able to hold the test position (loss of contact with the stadiometer for more than three seconds). The time during which the position was maintained was recorded. A good inter-session reproducibility (coefficient of variation lower than 8%) of this test in a student group has been reported by Demoulin et al. [26]. Strong and standardized verbal encouragements were provided during the various testing procedures. 2.3.2. Experimental session (S2) The first part of this session was the same as the familiarization session and identical for the EG and CG, i.e., all participants performed the warm-up phase and were installed as described previously. Thereafter, both groups performed the MVC test, which included the submaximal trials followed by a single MVC trial (pretest). Only one MVC trial was allowed for the posttest because additional trials would have increased the duration of the MVC test procedure and thereby in-

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C. Demoulin et al. / The Sørensen test is a fatiguing task

Fig. 1. Materials and methods: A: the harness; B: the chain used to link the ring harness to the strain gauge transducer; C: the MVC test; D: the Sørensen test. (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/BMR-150592)

fluenced the natural time course of recovery. Furthermore, a single trial was considered sufficient because all participants attended a familiarization session that included practicing MVC contractions. The chain was then unfastened and a three-minute rest was allowed for all subjects. Then, the participants in the EG and the CG performed the Sørensen test and rested, respectively. Both sessions were supervised by the same tester. 2.4. Statistical analyses The sample size was estimated using power-based sample size calculations. Based on an estimated standard deviation of 3 N·Kg−1 , the planned sample size was estimated at 40 participants per group to detect a 2 N·Kg−1 difference (δ) between groups on the retest when α is 0.05 and power is 80%. Skewness analyses and the Shapiro-Wilk test were performed to verify the assumption of normality of each variable. Descriptive analyses were undertaken and consisted of computing the mean (M ) and 95% confidence intervals (95% CI). Furthermore, an unpaired t-test was performed to compare the baseline characteristics and performances of the CG and EG.

A paired t-test combined with the intraclass coefficient correlation (ICC) (single measures SPSS output of the ICC analysis) and the standard error of measurement (SEM) calculation were conducted to establish whether the familiarization session (S1) was adequate by comparing the PF value of S1 and the single pre-test value of S2. The SEM was calculated as follows: √ SEM = SD × (1-R) with “SD” is the standard deviation of pre-test (S1) score and “R” is the test-retest reliability parameter. For the primary outcome, i.e., changes in the PF, a two-way analysis of variance (ANOVA) for repeated measures with groups as between-subjects factors was used to compare the pre- and post-test; a Student-Newman-Keuls was used for post-hoc analysis. Furthermore, Cohen’s effect sizes were calculated (Cohen’s d): M1 − M2 d=  2 2 SD1 +SD2 2

where M1 and M2 are the mean post-tests of relative PT in the EG and the CG, respectively, and SD1 and SD2 are the related standard deviations.

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Fig. 2. MVC force traces (and peak force) recorded before (pre-test) and after (post-test) a Sørensen test in a representative subject (a 70 kg male) of the experimental group. (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/BMR-150592)

The comparison of males and females regarding baseline characteristics and performances were conducted by means of an unpaired t-test. To compare fatigability following the Sørensen test between genders, a three-way analysis of variance (ANOVA) for repeated measures with groups as between-subjects factors and genders as an additional between-subjects factor was performed. The group effects on the change of relative PF were tested by an independent sample t test. Pearson correlation analyses were conducted to examine associations between pre-test PF value, percentage change in the PF (from pre-test to post-test) and time to task failure (whole group and males/females). All statistical analyses were performed with the Statistica computer package (Statsoft, Tulsa, Okla), and statistical significance was set at 0.05 for all analyses.

3. Results 3.1. Baseline data The participants included in the present study were 40 females (mean age: 22 years old (21.4–22.4)), mean weight: 59.2 kg (57.4–61.0) and mean height: 166.6 cm (164.7–168.4)) and 40 were males (mean age: 20.5 years old (19.8–21.1), mean weight: 73.5 kg (70.8–76.2) and mean height: 180.0 cm (178.1–182.7)). The descriptive statistics of the study sample are reported in Table 1.

Baseline comparisons between the CG and EG regarding the anthropometric values, the mean relative PF, and Sørensen holding time in the familiarization session did not reveal any statistical difference (P > 0.05) (Table 1). 3.2. Familiarization session The comparison between the MVC produced during S1 and the pre-test of S2 indicated no significant difference in relative PF in the CG group (mean 15.0 N·Kg−1 (13.9–16.0) vs. mean 14.8 N·Kg−1 (13.8–15.8), P = 0.23) and a slight decrease in the EG (mean 15.2 N·Kg−1 (14.3–16.1) vs. mean 14.7 N·Kg−1 (13.7–15.6), P = 0.02); the SEM calculated on the whole population was 0.926 N·Kg−1 whereas the ICC was 0.898. The mean holding time in the Sørensen test did not differ between S1 (mean 157.2 s (146.6–167.8)) and S2 (mean 159.7 s (148.0– 171.4); P = 0.39) in the EG; the SEM and ICC were 4.3 s and 0.867, respectively. No pain was reported by the participants either during the MVC tests or during the Sørensen test. 3.3. Fatigue assessment In the EG, the post-test was performed 13 ± 2 s after the end of the Sorensen test. The ANOVA related to the comparison between the relative PF in pre- and posttest for the EG and CG indicated a significant time effect with a significant group interaction (P < 0.0001). Indeed, for the CG, a slight but significant increase in

15.20 (14.32;16.08)

157.2 (146.6;167.8)

PF: peak force; CI: confidence intervals.

Sorensen (s)

Relative PF

173.0 (169.8;176.1)

Height (cm)

(N·kg−1 )

21.1 (20.5;21.7)

65.5 (62.0;69.0)

Weight (kg)

150.7 (136.3;165.1)

15.0 (13.96;16.04)

174.0 (171.0-177.0)

67.2 (64.2;70.2)

21.3 (20.6;22)

Mean (CI)

Mean (CI)

Age (years)

CG (n = 40)

EG (n = 40)

Whole population (n = 80)

0.46

0.82

0.63

0.45

0.61

P-value

147.0 (134.4;159.6)

16.24 (14.92;17.58)

180.5 (176.8;184.0)

73.2 (68.7;77.7)

20.6 (19.6;21.5)

Mean (CI)

EG (n = 20)

133.0 (118.4;147.6)

16.32 (14.96 ;16.70)

180.4 (177.2;183.6)

73.8 (70.4;77.2)

20.4 (19.4;21.4)

Mean (CI)

CG (n = 20)

Males (n = 40)

0.14

0.93

0.98

0.82

0.81

P-value

167.5 (150.5;184.4)

14.18 (13.10;15.24)

165.5 (163.2;167.8)

57.8 (55.6;60)

21.6 (21.0;22.3)

Mean (CI)

EG (n = 20)

168.4 (144.9;191.9)

13.68 (12.24;15.10)

167.6 (164.5;170.7)

60.6 (57.7;63.5)

22.2 (21.4;23.1)

Mean (CI)

CG (n = 20)

Females (n = 40)

Table 1 Baseline characteristics (means and confidence intervals) of the study population and their muscle performance recorded at the first session (S1)

0.95

0.56

0.27

0.11

0.25

P-value

36 C. Demoulin et al. / The Sørensen test is a fatiguing task

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relative PF occurred at S2 between the pre- and posttest (fatigue index: +2.7%, P = 0.001), whereas the mean relative PF was significantly reduced for the EG (fatigue index: −13%, P < 0.001; Fig. 2). These changes were associated with a large size effect (d = 0.87). At post-test, the between-group comparison showed a significantly lower value in relative PF in the EG compared to the CG (P = 0.0002). 3.4. Males vs. females The gender comparison in absolute and relative PF and in the Sørensen test holding time indicated significant differences at S1. Although the absolute and relative PF were significantly greater in males (P < 0.001), the mean holding time during the Sørensen test was significantly longer in females (mean 167.9 s (154.1–181.7) than in males (mean 140 seconds (130.5–149.5), P = 0.001). Similar differences between genders appeared at S2. Changes between time points in both females and males were similar to those of the population as a whole. A slight but significant increase in the CG (P -values: 0.028 and 0.034 in females and males, respectively) and a significant decrease in relative PF in the EG (P < 0.001 for both genders) were observed between the pre- and post-test values, with the relative PF being significantly lower than in the CG (P < 0.05) (Fig. 3). The ANOVA for repeated measures with groups and genders as a between factor showed a significant interaction effect of groups and genders (P = 0.032), with a fatigue index significantly greater in males than in females (−16.2% (−20.9; −11.5) vs. −9.7% (−14.1; −5.3), P = 0.044). The correlation analyses (whole group and males/ females) revealed no significant association (p > 0.05) between the pre-test PF value, percentage change in the PF (from pre-test to post-test) and time to task failure, except for the pre-test PF value which was correlated to the percentage change in the PF in the whole population (r = 0.31, p < 0.05), and between the latter and the time to task failure in males (r = 0.47, p < 0.05).

4. Discussion This study, which shows that the Sørensen test performed until failure in a young healthy population results in a reduced ability of the trunk extensor muscles to generate maximal force, indicates that this test is clearly a fatiguing task.

Fig. 3. Comparison between the pre- and post-test relative peak force (PF) of males and females within the experimental and the control groups (∗ P < 0.05; ∗∗∗ P < 0.001). (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/BMR-150592)

The Sørensen test, introduced a long time ago [1], has become a common test to assess trunk muscles function in patients with back pain and in athletes, as well in clinical practice as in the scientific community. Surprisingly, only few studies have investigated muscle fatigue induced by the test based on the decline of trunk extensors force [21,22,27–30]. In contrast to the study by Crowther et al. [21], a clear decline in MVC force occurred in our study following the Sørensen test. Despite a similar mean holding time and subjects’ ages, several factors may explain the discrepancy between studies. For example, the lack of familiarization with the procedures in Crowther et al.’ study might explain why six out of twenty participants doubled their torque after performing the Sørensen test [21]. In addition, the participant’s position for the MVC test (standing) and the time necessary to reinstall the participant on the dynamometric system may have contributed to underestimation of the effect of fatigue by allowing some recovery. As in our study, Champagne et al. [22] included a familiarization session and reported a significant decrease in force (−5.9% and −10.3% in young and elderly subjects, respectively). Several hypotheses related to methodological differences can be put forward to explain the fact that the decrease in force was more pronounced in the present study than in theirs: a) the difference in testing position (they used a modified version of the Sørensen test on a 45 degree Roman chair [22]); b) the greater number of MVC trials post-Sørensen test that were performed (four trials separated by a two-minute rest period in Champagne et al.’s study vs. a one-minute period in this study); c) the resulting longer resting

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period between the end of the Sørensen test and the last MVC trial allowing some recovery. The method they used to measure back extension MVC (maximal isometric lift test in a semi-crouching position) was also different from that in our study. By minimizing the time between the end of the Sørensen test and the post-MVC trial, our study indicates clearly that the Sørensen test induces fatigue of the trunk extensor muscles when performed until task failure. Considering the fact that PF was slightly lower at the pre-test of S2 than at S1 in the EG (suggesting a slight PF underestimation), the difference between groups might be even more significant. The slight (but significant) increase observed in the CG between pre- and post-test also suggests that, though the reproducibility parameters indicate that this MVC force measurement can be considered as reproducible, this measurement might be slightly influenced by some individual factors. As for other physical tests [31], fears, pain, and negative individual beliefs [32–34] might indeed influence performance. That could also explain the results of the correlation analyses between the percentage change in the PF and the time to task failure. As already reported in previous studies [2,12,25], a longer mean holding time was observed in this study for females than for males. The greater fatigability found in males is also in agreement with a greater change reported in most studies using S-EMG during the Sørensen test [12,25]. Several hypotheses have been proposed to explain this gender-related difference. First, the weight of the upper body is proportionally less in females than in males [2,35], meaning that a greater force must be generated to counteract the greater upper body weight in males [23]. The greater muscle mass necessary to maintain the trunk in the horizontal position in males might induce greater intramuscular pressures and thus a greater blood flow occlusion [36] than when females perform the same task, thereby reducing oxygen availability at the muscle level and metabolite washout. However, other mechanisms should also contribute to the greater fatigability in males than in females because genderrelated difference is also found when subjects perform an isometric endurance backward extension (“pulling test”) in standing position [35], and when males and females sustain the same relative MVC torque until failure [35,37]. A greater degree of lumbar lordosis in females has also been postulated (this may afford a mechanical advantage by lengthening the lever arm of the spinal erector muscles) [38,39]. Furthermore, differences in muscle composition have often been proposed

as a possible reason because spinal muscles may show better adaptation to aerobic exercise in females as a result of a greater proportion of Type I fibers [40]. However, a different fatigability between genders has also been reported when studying other muscles and tasks, particularly at low contraction intensities [23,41,42]. Considering that the magnitude of the difference to be attributed to gender seems to be specific to the task performed (lower when contractions are of low intensity, intermittent and performed by the elderly), these differences in fatigability cannot be explained by a single mechanism [43]. 5. Conclusions This study demonstrates that the Sørensen test performed until exhaustion in a young healthy population results in a decrease in the ability of the trunk extensor muscles to generate force, indicating that this test is clearly a fatiguing task. Considering that the Sørensen and trunk muscle strength tests are often included in physical test batteries used to assess trunk muscle performance [7,44], it is suggested that the Sørensen test be performed after the strength assessment of trunk extensor muscles or that sufficient recovery time be provided after the Sørensen test if it is followed by the strength test to avoid underestimation of the true muscle potential. Furthermore, the fatigue of the trunk extensor muscles induced by the Sorensen test appeared significantly more pronounced in males than in females confirming that reference values need to be different between genders. Acknowledgements The authors would like to thank Prof A. Tits, A. Depaifve, A. Mouton, D. Deflandre for their help, cooperation, and valuable assistance, as well as the participants who took part in the study. Conflict of interest This study received no commercial funding or other sponsorship and the authors confirm no conflicts of interest, financial or otherwise. References [1]

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Is the Sørensen test valid to assess muscle fatigue of the trunk extensor muscles?

Very few studies have quantified the degree of fatigue characterized by the decline in the maximal voluntary contraction (MVC) force of the trunk exte...
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