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Different Effect of Local and General Fatigue on Knee Joint Stiffness

WANG, DAN; DE VITO, GIUSEPPE; DITROILO, MASSIMILIANO; DELAHUNT, EAMONN

Medicine & Science in Sports & Exercise: January 2017 - Volume 49 - Issue 1 - p 173–182
doi: 10.1249/MSS.0000000000001086
APPLIED SCIENCES
Free

Purpose This study aimed to investigate the influence of locally and generally induced fatigue on the stiffness properties of the knee joint.

Methods Twenty-two male (24.9 ± 4.5 yr, 1.78 ± 0.06 m, 75.4 ± 6.4 kg, 23.9 ± 1.8 kg·m−2) and 18 female (21.1 ± 1.5 yr, 1.66 ± 0.05 m, 63.4 ± 6.5 kg, 22.9 ± 2.5 kg·m−2) amateur athletes participated. Peak torque (PT) of the knee extensor musculature, muscle stiffness (MS) of the vastus lateralis, and musculoarticular stiffness (MAS) of the knee joint were assessed pre- and postlocally and generally induced fatigue (undertaken on two separate days with a 1-wk interval).

Results Males were characterized by higher values of MAS, relaxed and contracted MS, normalized PT (PT/body mass), and normalized MAS (MAS/external load) irrespective of time point (P < 0.05).

Locally induced fatigue Contracted MS increased more (P < 0.01) and normalized PT decreased more (P = 0.03) in males than in females postfatigue. Significant increases occurred in MAS in females (P = 0.01); relaxed MS (males, P < 0.001; females, P < 0.001), contracted MS (males, P < 0.001; females, P = 0.04), and normalized MAS (males, P = 0.001; females, P = 0.01) in both sexes; and normalized contracted MS (contracted MS/external load) in males (P < 0.001). Normalized PT decreased significantly in males (P < 0.01) postfatigue.

Generally induced fatigue Contracted MS (P = 0.01) and MAS (P = 0.05) decreased significantly in males post-fatigue.

Conclusion The stiffness properties of the knee joint are influenced by locally and generally induced fatigue, with different responses being observed in males and females.

1School of Public Health, Physiotherapy and Sports Science, University College Dublin, Dublin, IRELAND; 2The No. 2 Clinical Medicine School, Nanjing University of Chinese Medicine, Nanjing, Jiang Su Province, CHINA; and 3Institute for Sport and Health, University College Dublin, Dublin, IRELAND

Address for correspondence: Dan Wang, M.Sc., A101 Health Sciences Centre, University College Dublin, Belfield, Dublin 4, Ireland; E-mail: dan.wang@ucdconnect.ie.

Submitted for publication May 2016.

Accepted for publication August 2016.

Muscle fatigue is considered as the inability of a muscle or a group of muscles to sustain a given task (30). It is associated with a reduction in maximum voluntary muscle force and is attributable to both central and/or peripheral mechanisms (30). Central fatigue refers to a progressive exercise-induced failure to activate a muscle voluntarily, which occurs above the neuromuscular junction (6,30), whereas peripheral fatigue implies a reduction in muscle force production due to exercise, which is located at or distal to the neuromuscular junction (6,30). Peripheral and/or central fatigue can be induced by exhaustive voluntary exercise (23). Generally speaking, muscular exercise can be performed as local muscular exercise (contraction of a particular muscular group) or general muscular exercise (mobilization of the whole body) (23). The manifestations of central fatigue and peripheral fatigue seem to be task dependent, and the type of exercise performed influences their roles in the development of muscle fatigue and also an individual’s recovery from its effects (6). Fatigue induced by local muscular exercise may cause dysfunction of muscle mechanoreceptors (19) and thus produce peripheral fatigue (23), whereas fatigue generated by general muscular exercise may diminish central nervous system sensorimotor control (19).

Stiffness is the relationship between an applied load and the elastic deformation of a biological structure (7). Muscle stiffness (MS) is defined as the ratio of the change in force to the change in muscle length (8), whereas musculoarticular stiffness (MAS) is a more comprehensive measurement of the whole joint, including stiffness of the muscle–tendon unit as well as skin, ligaments, and articular surfaces (7). All of the aforementioned biological structures have their own intrinsic properties, which contribute to MAS in a relaxed state (21). MS is modulated by the amount of muscle contraction and formed crossbridges and creates a link between joint mechanics and neuromuscular function under active conditions (21). MS and MAS have a fundamental purpose in the preparation and response to joint perturbations (21). They play an integral role in regulating and controlling human movement and, consequently, affect functional joint stability (21). In general, higher stiffness is beneficial to sports performance, but too little or too much stiffness may increase the risk of musculoskeletal injury (5). Taking running as an example, greater stiffness properties indicate less deformation of the structures (i.e., the stretch-shortening cycle has a more limited range of motion and thus more concentric force output at push-off), which may improve running economy and reduce the onset of fatigue (5). Appropriate levels of MS and MAS are necessary for optimal running, jumping, and hopping performance to absorb ground reaction forces and to store and reuse elastic energy (5).

The response of the stiffness properties of the human knee joint to fatigue varies in the published literature. A substantial decrease in knee muscle–tendon stiffness has been observed after the completion of two different fatigue protocols (consecutive sets of 10 repetitions of stretch-shortening cycle contractions; successive sets of 10 repetitions of isometric contractions for 10 s with the knee at 90° of flexion) (32). Distinct decreases in knee joint MAS have been observed after the completion of a fatiguing cycling protocol (8). This contrasts the findings of Sayers and Gardner (26) who observed an increase in knee joint stiffness in triathletes after the completion of a 40-km cycle. The divergent observations are likely the result of different fatigue protocols (general muscular exercise fatigue vs local muscular exercise fatigue) and MAS measurement techniques. To our knowledge, no study has compared and contrasted the influence of different fatigue protocols on the stiffness properties of the human knee joint.

Our previous work has identified that males are characterized by higher knee joint stiffness properties compared with females (33). Furthermore, significant decreases in knee joint MAS were identified in both sexes after the completion of a specific cycling fatigue protocol. However, cycling consists of repetitive, concentric-only muscle contraction and, therefore, has limited representativeness of sports participation. General exercises such as walking, running, and hopping are composed of concentric and eccentric muscle actions and have a different effect on knee joint sensorimotor control and stiffness. Considering the evidence, the influence of different mechanisms of induced fatigue (i.e., locally induced vs generally induced) on knee joint sensorimotor control, and in particular muscle and joint complex stiffness, warrants further investigation. Consequently, the aim of this study was to investigate the influence of two different fatigue protocols on the stiffness properties of the knee joint in amateur male and female athletes. It was hypothesized that the knee joint stiffness properties would respond differently to local and general fatigue protocols. On the basis of previous research, we theorized that local fatigue would increase the stiffness properties of the knee joint, with the opposite effect being observed after general fatigue (23).

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METHODS

Participants

Twenty-two male (age = 24.9 ± 4.5 yr, height = 1.78 ± 0.06 m, body mass = 75.4 ± 6.4 kg, body mass index [BMI] = 23.9 ± 1.8 kg·m−2) and eighteen female amateur athletes (age = 21.1 ± 1.5 yr, height = 1.66 ± 0.05 m, body mass = 63.4 ± 6.5 kg, BMI = 22.9 ± 2.5 kg·m−2) volunteered to participate. The University Human Research Ethics Committee approved the study protocol, and all participants signed consent forms. The specific inclusion criteria were as follows: 1) amateur athletes who participated in organized sports, 2) age 18–35 yr, 3) BMI ≤ 25 (if a participant’s BMI was >25, body fat ≤25% [males] or 35% [females], assessed via skinfold thickness, were deemed acceptable) (12), 4) no significant soft tissue injury to either lower limb in the last 6 months, and 5) no reported medical condition that could influence performance. Furthermore, participants were also screened using a medical history questionnaire (8) and the Physical Activity Readiness Questionnaire form.

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Study design

Each participant was required to visit our laboratory on three separate testing days. On day 1, each participant completed a familiarization protocol. On days 2 and 3, participants completed the isolated quadriceps fatigue (locally induced fatigue) protocol and the treadmill fatigue (generally induced fatigue) protocol, respectively, with a 1-wk interval in between. The following evaluations were performed before and after each fatigue protocol: 1) peak torque (PT) testing of their right knee joint extensor musculature, 2) relaxed MS testing of their right vastus lateralis (VL), 3) contracted MS testing of their right VL, and 4) contracted MAS testing of their right knee joint. On both days 2 and 3, participants were requested to attend the laboratory in a rested state, having been asked to maintain a normal diet and refrain from exercise in the preceding 24 h.

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Isolated quadriceps fatigue protocol (locally induced fatigue)

Participants performed 70 maximum effort right knee extensions at 90°·s−1 (continuous concentric–eccentric knee extension cycle mode without a pause between cycles) on an isokinetic dynamometer (Biodex System III; Biodex Medical System, Shirley, NY). A previous study (15) reported that 40–50 maximum effort knee extensions at 90°·s−1 performed on an isokinetic dynamometer were needed to fatigue the quadriceps. Seventy repetitions were selected according to the pilot tests in which participants reported satisfied levels of fatigue according to scores on the RPE scale (RPE ≥ 17). Participants were secured by pelvic and femoral straps and sat in the dynamometer chair with an angle of 110° between the alignment of the spine and the femur (15). Before the fatigue protocol, the participants performed a specific warm-up of 10 knee extensions at 90°·s−1 at 50% of their perceived maximum capability (20). During the protocol, verbal encouragement and visual feedback were provided; participants were required to perform maximum right knee concentric extension contractions as the arm of the dynamometer moved up from 75° flexion to 0° (1 s) and relax completely as the dynamometer arm moved back to 75° (1 s) (15). Torques were displayed on a computer monitor, and participants were encouraged to try to exceed their previously produced torque. RPE was recorded immediately after the locally induced fatigue protocol.

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Treadmill fatigue protocol (generally induced fatigue)

The treadmill fatigue protocol was used to induce whole-body fatigue. The treadmill fatigue protocol involved running with a constant grade of 1° of inclination. The protocol started at 8 km·h−1, and the treadmill speed was increased stepwise by 2 km·h−1 every 3 min. Participants were instructed to run until complete exhaustion (fatigued state, RPE ≥ 17), and verbal encouragement was given toward the end of each run. HR (HR monitor; Polar Electro Oy, Kempele, Finland) and subjective exertion (Borg scale) were assessed 30 s into each stage and immediately after the treadmill running test (29). The average time to exhaustion was 15.2 ± 2.5 min for males and 11.3 ± 1.9 min for females.

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PT

Each participant underwent PT testing of his or her right knee joint extensor musculature on a dynamometer (Bodymax Fitness, Clydebank, UK). The participant was seated on the dynamometer with their hip flexed at 105° and their right knee flexed at 80° (where full extension represents 0°) (7), with the lateral femoral condyle aligned with the axis of the dynamometer. The force transmission point was a bar that was positioned anteriorly to the participant’s lateral malleolus. The machine was equipped with a load cell (Leane International, Parma, Italy; measurement range = 0–500 kg, output = 2.00 mV·V−1) applied in series with the plane of force application. The load cell was secured to the leg extension machine with a chain. This prevented movements of the bar and therefore allowed an isometric contraction when the participant attempted to extend their leg. Participants were stabilized with straps at the pelvis to avoid movements toward hip extension during the test. Furthermore, to minimize any contribution from the upper body, participants were required to cross their hands across their body throughout. After familiarization with the procedures, participants were instructed to produce a maximum voluntary isometric contraction (MVIC) of their knee joint extensor musculature, as quickly as possible for approximately 3 s. Each participant was required to perform three MVIC, with the highest value recorded being used to determine the load with which MAS was assessed. During the performance of each MVIC, strong verbal encouragement and visual target stimulation were provided to motivate maximal contraction. The force signal was sampled at 1000 Hz and stored on a PC using a 16-bit A/D converter data acquisition system (Biopac Systems, Inc., Goleta, CA). The force signal was multiplied by the individual lever arm length to convert it into torque (N·m). The highest torque value was identified as PT, which was normalized to body mass of each individual (24) for further analysis.

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MS

MS of the VL muscle was measured using a device incorporating a probe and an accelerometer (Myometer, Myoton-3; Müomeetria AS, Tallinn, Estonia) sampled at 3200 Hz. During MS recordings, the subjects were seated in the same position used for MVIC measurements. The probe was manually positioned perpendicular to the muscle belly with the recording site being two-thirds the distance along a line measured from the anterior superior iliac spine to the midpoint on the lateral side of the patella. The probe was gently lowered onto the muscle belly of the VL with a resultant automatic mechanical effect being delivered to the muscle (a duration of 15 ms, a force of 0.3–0.4 N, and a local deformation in the order of a few millimeters) (7). The damped natural oscillations were recorded by the accelerometer within the probe giving an instantaneous digital output of the MS. Five consecutive measurements were taken during relaxed (no external load) and contacted (external load = 30% MVIC) conditions. The average of the five measurements was used for later analysis.

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MAS

The MAS of participants’ right knee joint was measured using a technique previously published by Ditroilo et al. (7). Participants sat in the same position used previously for MVIC assessments. To quantify submaximal MAS stiffness, the participants were required to support a load corresponding to 30% of MVIC on the anterior distal portion of their lower leg. An external perturbation of 100–150 N was applied to the bar by the investigator, and the ensuing oscillations were recorded by a uniaxial accelerometer (Crossbow, Milpitsa, CA) attached to the distal end of the lever arm of the leg extension dynamometer. Accelerometer data were sampled at 1000 Hz and recorded on a personal computer using a 16-bit A/D converter. A Butterworth low-pass filter (third order) with a cutoff frequency of 4 Hz was used to filter the signal. Each participant completed five MAS trials separated by a 1-min rest period, with the average of the three trials being used for analysis.

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Statistical analysis

A repeated-measures MANOVA was undertaken to investigate differences pre- and postfatigue between males and females on the following four dependent variables: 1) PT, 2) relaxed MS, 3) contracted MS, and 4) MAS, for each fatigue protocol. The independent variables were as follows: 1) time point (i.e., pre- and postfatigue) and 2) sex (i.e., male and female). Benjamini–Hochberg-type procedures were used for alpha-level adjustments (3). As stiffness is closely associated with the externally supported load, MAS and contracted MS were also normalized to individual external load to account for the sex differences in MVIC (7). An independent-samples t-test was conducted to investigate the difference in normalized MAS (MAS/external load) and normalized contracted MS (contracted MS/external load) between sexes pre- and postfatigue. Statistical significance was set a priori at P ≤ 0.05. Furthermore, a paired-samples t-test was conducted to investigate differences in normalized MAS and normalized contracted MS separately from pre- to postfatigue across sexes; the level of significance was set at P ≤ 0.05. Effect sizes were also calculated for each comparison. Statistical analyses were conducted in IBM SPSS Statistics 20 (IBM Ireland Ltd., Dublin, Ireland).

Sample size was calculated using G-Power version 3.0.10, ensuring a statistical power of 0.80, a two-tailed α of 0.05, and an effect size of 0.27 based on a previous study, which investigated the effect of a specific cycling fatigue protocol on the knee joint stiffness properties (unpublished data collected in our laboratory). The sample size needed was 33 participants. We recruited a conservative number of 40 participants to account for potential participant dropouts, missing data, and outliers.

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RESULTS

Isolated quadriceps fatigue protocol (locally induced fatigue)

A significant multivariate effect across the interaction between sex and time point (Pillai’s trace = 0.36, F4,35 = 4.95, P < 0.05, ŋp2 = 0.36) was reported. There was a significant between-subject multivariate effect for sex (on the combined four dependent variables, regardless of time point) (Pillai’s trace = 0.66, F4,35 = 17.26, P < 0.001, ŋp2 = 0.66). There was also a significant within-subject multivariate effect for time point (regardless of sex) (Pillai’s trace = 0.73, F4,35 = 23.82, P < 0.001, ŋp2 = 0.73).

Univariate between-group analyses showed that there were significant interactions between time point and sex for contracted MS (P < 0.01) and normalized PT (P = 0.03), but there were no interactions between time point and sex for MAS (P = 0.60) and relaxed MS (P = 0.38). The increase in contracted MS and the decrease in normalized PT postfatigue were greater for males than for females. Higher values of MAS (P < 0.001), relaxed MS (P = 0.04), contracted MS (P < 0.001), and normalized PT (P < 0.001) were observed in males than in females regardless of time point. Within-group univariate analyses indicated that MAS (P = 0.01), relaxed MS (P < 0.001), and contracted MS (P < 0.001) increased significantly postfatigue while normalized PT (P < 0.05) decreased significantly postfatigue irrespective of sex. When the normalization was implemented, significant differences between sexes in prefatigue MAS (P < 0.001) and postfatigue MAS (P < 0.001) were evident. Besides, significant increases were observed in normalized MAS in both males (P = 0.001) and females (P = 0.01). However, no significant differences were observed in normalized contracted MS between sexes prefatigue (P = 0.06) and postfatigue (P = 0.84), whereas a significant increase in contracted MS was only observed in males (P < 0.001) but not females (P = 0.09) postfatigue. Details of the differences in the between- and within-group comparisons are presented in Table 1 as well as Figures 1 and 3.

FIGURE 1

FIGURE 1

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Treadmill fatigue protocol (generally induced fatigue)

There was no significant multivariate effect across the interaction between sex and time point (Pillai’s trace = 0.09, F4,35 = 0.91, P = 0.47, ŋp2 = 0.09). There was a significant between-subject multivariate effect for sex (on the combined four dependent variables, regardless of time point) (Pillai’s trace = 0.61, F4,35 = 13.38, P < 0.001, ŋp2 = 0.61). There was also a significant within-subject multivariate effect for time point (regardless of sex) (Pillai’s trace = 0.26, F4,35 = 3.07, P = 0.03, ŋp2 = 0.26).

Univariate between-group analyses showed a higher value of MAS (P < 0.001), relaxed MS (P = 0.04), contracted MS (P < 0.001), and normalized PT (P < 0.001) in males than in females regardless of time point. Within-group univariate analyses indicated that contracted MS (P < 0.05) decreased significantly after fatigue, whereas MAS (P = 0.11), relaxed MS (P = 0.44), and normalized PT (P = 0.22) did not change significantly after fatigue irrespective of sex. However, because the change of MAS is of pivotal importance in this study, a paired-samples t-test was conducted and revealed that MAS in males significantly decreased from pre- to postfatigue (P = 0.05). When the normalization was implemented, significant differences between sexes in prefatigue MAS (P < 0.001) and postfatigue MAS (P < 0.05) were evident. No significant increases were observed in normalized MAS in both males (P = 0.21) and females (P = 0.77) postfatigue. No significant differences were observed in normalized contracted MS between sexes prefatigue (P = 0.13) and postfatigue (P = 0.16), furthermore, no significant increase in contracted MS was observed in males (P = 0.65) and females (P = 0.36) postfatigue. Details of the differences in the between- and within-group comparisons are presented in Table 2 as well as Figures 2 and 3.

FIGURE 2

FIGURE 2

FIGURE 3

FIGURE 3

TABLE 1

TABLE 1

TABLE 2

TABLE 2

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DISCUSSION

The purpose of this study was to investigate the influence of two different fatigue protocols on the stiffness properties of the knee joint in amateur male and female athletes. An isolated quadriceps fatigue protocol and a treadmill running fatigue protocol were used to induce local and general fatigue, respectively.

Males demonstrated higher MAS and contracted MS values relative to their female counterparts, before and after completion of both fatigue protocols. As described by Needle et al. (21), active muscle–tendon stiffness is the dominant component when considering total joint stiffness and, hence, MAS. Indeed, volitional muscle contraction can increase joint stiffness by more than fourfold. Consequently, factors related to muscle force production, such as muscle mass, muscle fiber type, and muscle activation characteristics (24), are promising explanations for the observed sex differences in MAS. In addition, knee joint stiffness properties can also be influenced by hormones specifically free testosterone (2). Early studies have shown that when compared with females, male adults possess approximately seven to eight times more free testosterone (27). Bell et al. (2) have also reported that a negative relationship exists between estrogen and MAS, offering some explanation for the lower MAS observed in females. We can speculate that this is a contributing factor for the observed results in the present study. After the implication of normalization, significant differences were noticed in MAS, but not in contracted MS between sexes, before and after both fatigue protocols. The fact that sex differences in contracted MS were not apparent after normalization to external load suggests that sex differences in MVIC likely contribute to sex differences in contracted MS. In addition, males and females might have different stiffness properties in passive structures around the joint as well as varying peripherally mediated and centrally mediated reactions in response to local fatigue.

Sex differences in MS may be explained by the fact that males have a larger physiological cross-sectional area, more muscle mass, and thus a greater amount of muscle fiber crossbridges (4) and titin (33). The formation of crossbridges between actin and myosin filaments in the overlap regions is the main determinant of MS, whereas the fiber-type composition and muscle architecture are also contributors to the generation of MS (7). Ditroilo et al. (7) summarized that more type I fibers, and a decrease in fiber length would indicate a higher level of MS, whereas a decrease in pennation angle would account for a reduction in MS. Males are characterized by larger cross-sectional area of type I fibers (28), shorter relative fascicle lengths (to limb length) of the VL, and greater pennation angles than females (14). Furthermore, increased muscle mass in males implies more passive connective tissue and, hence, a greater number of collagen fibers for lengthening resistance, leading to increased MS (4).

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Isolated quadriceps fatigue (locally induced fatigue)

After the completion of the isolated quadriceps fatigue protocol, relaxed MS and contracted MS increased significantly in both sexes, whereas MAS increased significantly in females but not in males. In addition, normalized PT decreased significantly in males but not in females.

Relaxed and contracted MS increased discernibly after the completion of the isolated quadriceps fatigue protocol. The local contractile fatigue induced by the isolated quadriceps fatigue protocol could be attributed to intramuscular metabolite accumulation, such as inorganic phosphate (Pi) and H+ (6). A decrement in pH and free energy of ATP hydrolysis resulted in slowing crossbridge cycling and a reduction in Ca2+ uptake (34). These are all contributors to a slowing of muscle relaxation. In addition, Hotta and Ito (13) suggested that the accumulation of muscle fatigue actually generates MS and muscle tension despite an acute reduction in muscle strength. The mechanisms for this phenomenon can be attributed to the acidification induced by fatigue, which makes the myosin crossbridges adhere more firmly to the titin filaments (34). Another possible mechanism for the observed increase in MS is that the development of local fatigue may act as a trigger for an increase in central drive and a resultant rise in the firing rate of and/or recruitment of motor units. This may occur to compensate for the contractile fatigue to satisfy the required workload (1,6).

These explanations are also applicable to the postfatigue increment of MAS observed in females. However, although postfatigue MAS in males did not change significantly, they were observed to exhibit a substantially greater increment in contracted MS than their female peers (males = 28.70% increase, females = 7.02% increase). This could be because males have greater muscle mass and thus greater metabolic demand and rely more on anaerobic metabolic pathways compared with females (17). Accordingly, males are expected to incur greater fatigue because of the by-products generated by these pathways (25); therefore, in comparison with females, males exhibited a greater magnitude of increase in contracted MS. In light of one previous study (10), males exhibit less relative fatigue resistance than females, the mechanisms of which can be classified into the following themes: 1) higher absolute muscle forces when performing the same relative work as females, 2) greater glycolytic capacity and a greater reliance on glycolytic pathways than females, and 3) higher proportions of the more fatigable type II fibers in the VL compared with females (17). Interestingly, males incurred a greater impairment in neuromuscular activation than females after the fatigue protocol. Because of the greater fatigue observed in males (as evidenced by a higher % decrement in PT), it is plausible that lower-limb maximal voluntary contractions contribute greater inhibition to central motor drive in males compared with females. This could contribute to the nonsignificant alteration of MAS in males (25). After normalization, the significant postfatigue increase in contracted MS in females was rendered nonsignificant, whereas the nonsignificant postfatigue increase in MAS in males was rendered significant. This could further confirm that males accumulated more by-products induced by fatigue than females, and central fatigue was not triggered yet in males and females after local fatigue.

Normalized PT decreased significantly in males but not in females postfatigue. In the contractile process, Ca2+ is an essential factor that leads to muscle contraction when released from the sarcoplasmic reticulum (SR) and muscle relaxation when removed from the contractile proteins back into the SR by the SR Ca2+-ATPase (11). Postacute high-intensity exercise or prolonged exercise, Ca2+ uptake has been observed to be decreased in a healthy male population (9). Another possible outcome of contractile fatigue is the fall in the phosphorylation potential, which is suggested by a greater rise in free Pi, free adenosine diphosphate, and monophosphate (6). Our observation of decreased normalized PT of the knee extensor muscles is in accordance with the findings of Hill et al. (11), in which there was a significant decrease in MVIC of the knee extensor muscles after an intense, isokinetic leg kicking exercise. This leg kicking exercise included two sets of 90 repetitions at a speed of 240°·s−1 for extension and 60°·s−1 for flexion. Each repetition took approximately 2.3 s with the leg extending from 100° to 0° for 0.5 s and relaxing for flexion back to 100° for 1.8 s. In our study, each repetition was approximately 2 s (1 s for extension and flexion, respectively). In addition, a previous study (24) suggested that healthy young males displayed a faster rate of knee extensor torque fatigue and slower recovery from fatigue compared with females. Pincivero et al. (24) attributed muscle fiber–type proportion, cross-sectional area, and oxidative potential, as previously outlined (17), to the mechanisms of discrepancy in sex-specific muscle fatigue patterns. These theories support the results of our study, which showed a significant decrease in normalized PT and a greater decrease of normalized PT in males compared with females postfatigue.

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Treadmill fatigue (generally induced fatigue)

After the treadmill fatigue protocol, contracted MS and MAS decreased significantly, with the rest of the variables (relaxed MS and normalized PT) showing no significant changes. A study, which also used a treadmill fatigue protocol, reported that the mean RPE of participants at exhaustion was 19.5 ± 0.6 and that their mean maximum HR was 194.3 ± 8.2 bpm (29). Participants in our study reached a similar level of fatigue after the completion of this treadmill fatigue protocol: mean RPE at exhaustion was 18.8 ± 1.3 for males and 18.0 ± 1.3 for females, and mean maximal HR was 191.1 ± 7.8 bpm for males and 188.3 ± 8.2 bpm for females.

A considerable body of research has indicated that there are sex disparities in the proportion of centrally and peripherally mediated fatigue after exhausting exercise; however, the conclusion is controversial as a result of the diversity of protocols (e.g., intermittent vs continuous), exercise mode (e.g., isometric contractions vs dynamic whole-body exercise), and muscles investigated (e.g., elbow flexors vs knee extensors) in different studies (31). Females generally exhibit a greater relative fatigue resistance than males (10). The potential explanations for this phenomenon could be the sex differences in anthropometrics, the effects of reproductive hormones in females, and the sex differences in substrate use, tendon characteristics, and running biomechanics (31).

The development of peripherally mediated fatigue happens early, whereas the occurrence of centrally mediated fatigue occurs toward the end of exercise and typically coincides with task failure (6). Amann and Dempse (1) reported that whole-body endurance exercise performance is determined to a significant extent by the feedback effects of peripheral muscle fatigue on central motor output. This means that when contractile impairment starts, recruitment of additional motor units and/or enhanced motor neuron firing rate are increased via central motor command. However, once a critical degree of central fatigue level is reached, no further increase in central command occurs, and central fatigue has commenced at this point (6). Contractile components play an important role in contracted MS and MAS, and they are activated by the central nervous system (7,21). Accordingly, the central fatigue induced by a running fatigue protocol influenced males to a greater extent, which can be seen in the significant decrease in the value of contracted MS and MAS. However, with the volitional muscle activity absent, relaxed MS is largely determined by the resting muscle tone, which exists unconsciously and controls the tautness of a relaxed muscle (21). Hence, it remained at a similar level after the exhaustion from running. The significant differences of contracted MS and MAS from pre- to postfatigue in males were diminished by normalization to external load, but PT did not change significantly after the completion of the treadmill fatigue protocol. This indicates that the centrally mediated fatigue induced by treadmill protocol might be attenuated through normalization; besides, stiffness changes elicited by generally induced fatigue were not as much as those elicited by locally induced fatigue.

As for normalized PT, there is speculation that there could be a central protective mechanism, which means that the central nervous system would limit muscle work during prolonged running to prevent extensive homeostasis disturbance, muscle damage, and biological harm (18). Central fatigue would minimize the extent of peripheral fatigue, and very limited peripheral alterations have been reported after 24 h treadmill running (16). Although the average time to exhaustion for participants in this study was 15.2 ± 2.5 min for males and 11.3 ± 1.9 min for females, central nervous system fatigue already contributes to the fatigue during prolonged exercise lasting from tens of minutes to hours (22). Therefore, the postfatigue normalized PT did not change significantly in both sexes. Furthermore, Miura et al. (19) also detected proprioceptive decline without muscle weakness of the knee after 5 min of running at 10 km·h−1 on a treadmill with a 10% uphill grade, suggesting a change in the central nervous system pathway without influence from muscle mechanoreceptors.

In conclusion, after local fatigue (isolated quadriceps fatigue protocol), relaxed and contracted MS increased significantly in both males and females; there was also a significant increase in MAS and a significant decrement in normalized PT in females but not in males. However, after general fatigue (treadmill fatigue protocol), contracted MS and MAS decreased significantly in males with a nonsignificant alteration of residual variables in both sexes. The findings from this study indicate that local fatigue and general fatigue generate diverse influences on the stiffness properties of the knee joint with both sexes responding differently to each other according to each fatigue protocol.

Dan Wang was supported by a research studentship from the China Scholarship Council. For the remaining authors, none were declared. The authors thank Ms. Sonja Egan, Ms. Alice O’Dwyer, Ms. Catriona Molony, and Ms. Karen O’Hare, who were students in School of Public Health, Physiotherapy and Sports Science, University College Dublin, for their help in the female participants’ recruitment and data collection.

The results of this study do not constitute endorsement by the American College of Sports Medicine, and they are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation.

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REFERENCES

1. Amann M, Dempsey JA. Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol. 2008;586(1):161–73.
2. Bell DR, Blackburn JT, Norcorss MF, et al. Estrogen and muscle stiffness have a negative relationship in females. Knee Surg Sports Traumatol Arthrosc. 2012;20(2):361–7.
3. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat. 2001;29(4):1165–88.
4. Blackburn JT, Riemann BL, Padua DA, Guskiewicz KM. Sex comparison of extensibility, passive, and active stiffness of the knee flexors. Clin Biomech (Bristol, Avon). 2004;19(1):36–43.
5. Brazier J, Bishop C, Simons C, Antrobus M, Read PJ, Turner AN. Lower extremity stiffness: effects on performance and injury and implications for training. Strength Cond J. 2014;36(5):103–12.
6. Decorte N, Lafaix PA, Millet GY, Wuyam B, Verges S. Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scand J Med Sci Sports. 2012;22(3):381–91.
7. Ditroilo M, Cully L, Boreham CA, De Vito G. Assessment of musculo-articular and muscle stiffness in young and older men. Muscle Nerve. 2012;46(4):559–65.
8. Ditroilo M, Watsford M, Fernandez-Pena E, D’Amen G, Lucertini F, De Vito G. Effects of fatigue on muscle stiffness and intermittent sprinting during cycling. Med Sci Sports Exerc. 2011;43(5):837–45.
9. Gollnick PD, Korge P, Karpakka J, Saltin B. Elongation of skeletal-muscle relaxation during exercise is linked to reduced calcium-uptake by the sarcoplasmic-reticulum in man. Acta Physiol Scand. 1991;142(1):135–6.
10. Hicks AL, Kent-Braun J, Ditor DS. Sex differences in human skeletal muscle fatigue. Exerc Sport Sci Rev. 2001;29(3):109–12.
11. Hill CA, Thompson MW, Ruell PA, Thom JM, White MJ. Sarcoplasmic reticulum function and muscle contractile character following fatiguing exercise in humans. J Physiol. 2001;531(Pt 3):871–8.
12. Ho-Pham LT, Campbell LV, Nguyen TV. More on body fat cutoff points. Mayo Clin Proc. 2011;86(6): 584; author reply 585.
13. Hotta Y, Ito K. Detection of EMG-based muscle fatigue during cyclic dynamic contraction using a monopolar configuration. Conf Proc IEEE Eng Med Biol Soc. 2013;2013:2140–3.
14. Kubo K, Kanehisa H, Azuma K, et al. Muscle architectural characteristics in young and elderly men and women. Int J Sports Med. 2003;24(2):125–30.
15. Larsson B, Karlsson S, Eriksson A, Gerdle B. Test-retest reliability of EMG and peak torque during repetitive maximum concentric knee extensions. J Electromyogr Kinesiol. 2003;13(3):281–7.
16. Martin V, Kerherve H, Messonnier LA, et al. Central and peripheral contributions to neuromuscular fatigue induced by a 24-h treadmill run. J Appl Physiol. 2010;108(5):1224–33.
17. Miller AE, MacDougall JD, Tarnopolsky MA, Sale DG. Gender differences in strength and muscle fiber characteristics. Eur J Appl Physiol Occup Physiol. 1993;66(3):254–62.
18. Millet GY, Lepers R. Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med. 2004;34(2):105–16.
19. Miura K, Ishibashi Y, Tsuda E, Okamura Y, Otsuka H, Toh S. The effect of local and general fatigue on knee proprioception. Arthroscopy. 2004;20(4):414–8.
20. Murdock GH, Hubley-Kozey CL. Effect of a high intensity quadriceps fatigue protocol on knee joint mechanics and muscle activation during gait in young adults. Eur J Appl Physiol. 2012;112(2):439–49.
21. Needle AR, Baumeister J, Kaminski TW, Higginson JS, Farquhar WB, Swanik CB. Neuromechanical coupling in the regulation of muscle tone and joint stiffness. Scand J Med Sci Sports. 2014;24(5):737–48.
22. Noakes TD. Physiological models to understand exercise fatigue and the adaptations that predict or enhance athletic performance. Scand J Med Sci Sports. 2000;10(3):123–45.
23. Paillard T. Effects of general and local fatigue on postural control: a review. Neurosci Biobehav Rev. 2012;36(1):162–76.
24. Pincivero DM, Gandaio CM, Ito Y. Gender-specific knee extensor torque, flexor torque, and muscle fatigue responses during maximal effort contractions. Eur J Appl Physiol. 2003;89(2):134–41.
25. Russ DW, Kent-Braun JA. Sex differences in human skeletal muscle fatigue are eliminated under ischemic conditions. J Appl Physiol. 2003;94(6):2414–22.
26. Sayers M, Gardner B. The effect of prior cycling on leg stiffness during running in high performance triathletes. 30th Annual Conference of Biomechanics in Sports, 2012, Jul 2–6. Melbourne (Australia). 2012. pp. 22–5.
27. Southren AL, Tochimoto S, Carmody NC, Isurugi K. Plasma production rates of testosterone in normal adult men and women and in patients with the syndrome of feminizing testes. J Clin Endocrinol Metab. 1965;25(11):1441–50.
28. Staron RS, Hagerman FC, Hikida RS, et al. Fiber type composition of the vastus lateralis muscle of young men and women. J Histochem Cytochem. 2000;48(5):623–9.
29. Steib S, Hentschke C, Welsch G, Pfeifer K, Zech A. Effects of fatiguing treadmill running on sensorimotor control in athletes with and without functional ankle instability. Clin Biomech. 2013;28(7):790–5.
30. Taylor JL, Gandevia SC. A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol. 2008;104(2):542–50.
31. Temesi J, Arnal PJ, Rupp T, et al. Are females more resistant to extreme neuromuscular fatigue? Med Sci Sports Exerc. 2014;47(7):1372–82.
32. Toumi H, Poumarat G, Best TM, Martin A, Fairclough J, Benjamin M. Fatigue and muscle–tendon stiffness after stretch-shortening cycle and isometric exercise. Appl Physiol Nutr Metab. 2006;31(5):565–72.
33. Wang D, De Vito G, Ditroilo M, Fong DT, Delahunt E. A comparison of muscle stiffness and musculoarticular stiffness of the knee joint in young athletic males and females. J Electromyogr Kines. 2015;25(3):495–500.
34. Zhang LQ, Rymer WZ. Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. J Neurophysiol. 2001;86(3):1086–94.
Keywords:

MUSCLE–TENDON UNIT; ELASTICITY; BIOMECHANICAL PHENOMENA; NEUROMUSCULAR; CENTRAL NERVOUS SYSTEM; PERIPHERAL NERVOUS SYSTEM

© 2017 American College of Sports Medicine