Recovery from a 1-minute bout of fatiguing exercise: characteristics, reliability, and responsiveness.

[Sinacore DR, Bander BL, DeLitto A. Recovery from a 1-minute bout of fatiguing exercise: characteristics, reliability, and responsiveness. Phys Ther 1994; 74:234-244.]

Key Words: Exercise, general, Fatigue, Muscle performance, lower extremity,

The assessment of local muscle endurance presents a perplexing clinical challenge for rehabilitation professionals. ideally, clinicians would like a measure of fatigue or endurance capacity (of an individual muscle or group of muscles) that can indicate changes in a muscle's ability to produce and maintain torque over a prescribed period of time. Preferably, such a muscle fatigue measure would be highly reflective of and responsive to any changes induced in the muscle(s) due to exercise or disease. To date, such a fatigue measure has not been described. Although many different types of measures have been suggested,[1] none have demonstrated the ability to discriminate the physiological adaptations that are associated with improvements in local muscle endurance.[2]

Some voluntary tests of muscle fatigue may be methodologically flawed, which can make interpretation of the test results difficult, if not impossible. Other muscle fatigue measures may be methodologically sound, but theoretically flawed and not reflective of any muscle fatigue construct (ie., not valid measures of muscle fatigue). To illustrate these points, we will discuss some select methodological problems and theoretical concerns about two commonly used voluntary tests of muscle fatigue.

One commonly used test of local muscle endurance of the quadriceps femoris muscle was first described by Thorstensson and Karlsson.[3] They defined a fatigue index as the decline in force (torque) after 50 repeated maximal isokinetic movements at 180[degrees]/s, and they expressed the index as a percentage of the initial torque values. Thorstensson and Karlsson demonstrated that their fatigue index reflected the percentage of fast-twitch muscle fibers in the vastus lateralis muscle of a small group of college-age students.

Although Thorstensson and Karlsson's test[3] was not originally intended to reflect adaptive changes in quadriceps femoris muscle endurance due to exercise or disease, clinicians have adopted the test and used the fatigue index with such an expectation. Therefore, we believe that the clinical use of Thorstensson and Karlsson's test and fatigue index measure is theoretically flawed and that they may not be valid measures of muscle fatigue or endurance. Our theoretical concerns are not with the test or the fatigue index as described, but rather with the clinical application and utility of this test by rehabilitation professionals. The fatigue protocol described by Thorstensson and Karlsson appears to be methodologically sound because the authors strictly controlled for joint excursions, the number of repetitions performed, the rate of muscle contractions, and the endpoints of the test and they tested only one muscle group during a single test. Unfortunately, studies assessing the validity and responsiveness of the fatigue index (or similar modifications of this test) have yet to be reported.

A common difficulty with many measures of voluntary muscle fatigue is the high degree of variability in the rate and extent of torque (force) decline. A high degree of variability in the rate or extent of torque decline makes the interpretation of any fatigue measure problematic, because it is difficult to discern any changes.

One modification of the fatigue index protocol was made in the endpoint of the test. This modification, which was originally described in the Cybex II[R] isokinetic dynamometer(*) manufacturer's handbook on isokinetics[4] and suggested for clinical use,[5] is particularly variable. Not only have we found this fatigue test to be unreflective of any patient's complaints of fatigue, but it is highly unresponsive to changes resulting from endurance exercise training programs (both theoretical flaws). The endpoint of this test is based on the number of repetitions completed until torque declines to 50%.

We attribute this measure's shortcomings to the high degree of variability, largely from fluctuations in the endpoint of the test (a methodological flaw), although a lack of standardization in controlling the rate of maximal contractions and the magnitude of joint excursions may also contribute. Similarly, there is little physiological rationale offered for terminating the test at 50% of initial torque values as the endpoint (a theoretical flaw). Another potential confounding variable with this protocol is the common practice of testing reciprocal muscle groups during a single fatigue test (eg, knee extensors and knee flexors).[5] This practice may contribute to variability in the test, as well as compromise true indications of muscle fatigue, especially if corrections for both the weight of the limb and lever arm against and with gravity are not used.[6]

We believe some commonly encountered clinical examples help illustrate these shortcomings. One example involves rehabilitation of a patient population, and another involves the use of endurance exercises to train subjects without muscle pathology. First, consider fatigue testing a patient's knee extensor muscles shortly after knee surgery and comparing the involved and uninvolved musculature. The initial torque values of the uninvolved muscles usually far exceed those of the involved side, resulting in a smaller number of repetitions to the 50% criterion in the uninvolved musculature. This results in the appearance of greater fatigue in the uninvolved musculature, a finding that rarely corroborates the patient's complaints or relates to functional deficits and that causes us to suspect the utility of such a test for sensing changes in the muscle's ability to produce and maintain a given torque level over a prescribed time a theoretical flaw).

Additionally, the endpoints of both fatigue tests described previously appear to be highly dependent on an individual's level of initial torque output (a methodological flaw). Individuals with initially high torque outputs routinely appear more fatigued (ie, less able to maintain a percentage of their initial torque output) than individuals with moderate or lower initial peak torque outputs, a finding that is difficult to interpret (a theoretical flaw).

Another example is the subject who has no obvious muscle deficits, but who trains with endurance exercise and presumably improves local muscle endurance. We often find that such individual's initial peak torque may decline considerably after programs of intense endurance exercise training, resulting in analogous declines in the 50% criterion to terminate the test. These findings lead us to believe that fatigue tests with endpoints that are dependent on obtaining some percentage of the initial torque output become difficult to interpret. Such fluctuations in the test's fundamental criteria also raise serious concerns, especially in a test-retest situation in which we question whether we are administering the same test on the second occasion because the endpoint has changed.

Due to the limitations in fatigue indexes based on percentage of decline, we have adopted using recovery of muscle peak torque (force) after a standardized bout of fatiguing exercise as an indicator of local muscle endurance. We acknowledge the recovery of muscle torque may be assessing a different physiological system[7,8] and perhaps a different metabolic pathway[9-13] than the rate of torque decline, but we contend the rate of muscle torque recovery is less variable than percentage of peak torque decline. Recovery of muscle peak torque is based on volitional effort and is derived from the percentage of initial torque at the start of the test. In our experience, however, recovery appears to be independent of the magnitude of initial torque output. Further, our experience dictates that the measurement characteristics (eg, adequate test-retest reliability) of peak torque recovery equal or exceed those of percentage-of-decline measures. These facts may make the recovery of muscle torque a more responsive measure of muscular adaptive changes than are percentage-of-decline measures.

The purposes of our study were (1) to describe the characteristics of recovery from a 1-minute bout of fatiguing isokinetic exercise of the quadriceps femoris muscle, (2) to assess the short-term reliability of the recovery of peak torque and percentage of decline in peak torque at the end of the test, and (3) to determine whether the recovery of local muscle torque more closely associates with maximal endurance exercise capacity than the percentage of decline in torque at the end of a fatigue test.

Method

Design

The overall design of this study consisted of two phases. In phase 1, we conducted a reliability assessment of two measures of local quadriceps femoris muscle fatigue--the percentage of decline in torque at the end of the fatigue test and the recovery of muscle torque at 30-second intervals for 4 minutes--in a group of nondisabled subjects. Using a different group of nondisabled subjects in phase 2, we next conducted a correlational analysis of both local muscle fatigue measures as well as a central measure of endurance capacity, maximal oxygen uptake ([VO.sub.2]max). We hypothesized that the recovery of muscle peak torque would be the less error prone of two local fatigue measures and, partially because of its better measurement properties, would account for more of the variability of the central endurance measure.

Our rationale for using [VO.sub.2]max as a criterion measure was not to specifically assess which of the local measures of fatigue would best predict cardiovascular endurance. Instead, we attempted to compare and contrast local muscle fatigue measures with a central measure of total-body muscle endurance using the measure of [VO.sub.2]max in a construct validation approach as the "criterion" measure. Our underlying assumption was that the central measure of maximal aerobic exercise capacity should significantly correlate with local measures of quadriceps femoris muscle fatigue. The use of [VO.sub.2]max as a criterion to reflect changes in local muscle fatigue can be justified by a number of reports, which suggest at least 50% of the observed increases resulting from endurance-types of exercise training are due to an enhanced local skeletal muscle respiratory capacity.[2]

We therefore purposely selected subjects with a wide range of maximal endurance exercise capacities. The subjects' [VO.sub.2]max values ranged from 29.9 to 75.5 mL/kg/min. Specifically, we studied individuals who participate regularly in endurance training activities, either bicycling or running, both being predominantly lower-extremity activities that necessitate repetitive quadriceps femoris muscle activity and are likely to induce exercise-induced adaptations.

Subjects

Thirty-three nondisabled subjects, ranging in age from 23 to 34 years ([bar] X=27, SD=3.4), volunteered to participate in the reliability portion phase 1) of this study (Tab. 1). Eighteen of these subjects were male (mean age=27 years, SD=3.7 years), and 15 were female (mean age=26 years, SD=3.0 years). Subjects were selected from individuals associated with two local metropolitan hospital communities. No criteria for participation were included, other than the subjects were asked to agree to an initial fatigue test and retest within a 7-day period.

[TABULAR DATA 1 OMITTED]

In the correlational phase of the study (phase 2), a different group of 21 nondisabled subjects, ranging in age from 21 to 47 years ([bar] X=27.5, SD=5.2), volunteered to perform a single fatigue test and have their maximal aerobic exercise capacity ([VO.sub.2]max) assessed on a treadmill or bicycle ergometer (Tab. 1). Every attempt was made to solicit the participation of any subject who could complete a single fatigue test and a [VO.sub.2]max test, regardless of the subject's level of regular physical activity. Nondisabled subjects were selected in order to study the characteristics of local muscle torque recovery in individuals without acute or chronic primary or secondary muscle deficits. All subjects signed an informed consent form outlining the study procedures.

Procedure

Fatigue test and recovery. All subjects performed a fatigue test of the left quadriceps femoris muscle that consisted of 50 repeated, maximal isokinetic knee extensions at 180[degrees]/s on a Cybex[R] II isokinetic dynamometer as previously described by Thorstensson and Karlsson.[3] Subjects were seated with their hips between 75 and 90 degrees of flexion. The axis of rotation of the isokinetic dynamometer was aligned with the anatomical axis of the subject's knee, and the lever arm was attached to the subject's leg at a distance of approximately 70% of the length from the medial knee joint line to the medial malleolus to allow for a standardized and comfortable site. The subject's thigh was stabilized with a canvas strap fixed to the table. Subjects were asked to maximally extend their leg through a complete range of 90 degrees and were paced at a rate of 50 extensions per minute by use of a metronome. The 90-degree range was maintained by mechanical stops to ensure a consistent arc of motion.

To assess the rate of muscle torque recovery, each subject performed a single maximal knee extension every 30 seconds for 4 minutes of recovery. Several subjects continued performing a single knee extension every 30 seconds for 10 minutes of recovery, The percentage of decline in torque after 1 minute and at every 30-second interval of recovery was calculated and expressed as a percentage of the initial peak torque at the start of the fatigue test).

The initial peak torque was derived from the average of the first three knee extensions that did not vary significantly from the mean of three single knee extension contractions performed prior to the fatigue test. The final peak torque was the average of the 46th through 50th knee extensions. Peak torque was obtained from a dual-channel strip chart recorder using a damp setting of 2, which remained constant for all tests. Corrections for lifting the weight of the limb and lever arm against gravity were not added to the obtained peak torques, because average differences in gravity-corrected and -uncorrected values have been reported to be small (ie, 2.4%).[6] The effect of not correcting our data for the percentages calculated in our study, however, was not determined. Calibration of the dynamometer was performed with known loads of 13.65 and 36.85 kg at 180[degrees]/s prior to each test.

The retest was performed in the exact manner as described. In an attempt to control variability and reproduce peak isokinetic torque, subjects were instructed to report at the same time of day for retesting. The time of day for the starts of the initial test and retest were recorded and did not vary by more than 15 minutes. Similarly, all subjects were asked to recall and record all dietary intake and timing of food intake on the initial testing day.

Subjects were asked to reproduce exact dietary intake and timing of meals on the day of the fatigue retest. No effort was made to limit or alter dietary intake. The mean test interval was 5 days, with a range of 3 to 7 days. We wanted to assess the muscle performance variables over a short time period, so we selected a 7-day maximal interest interval so as not to have residual effects from the initial isokinetic exercise, yet minimize any potential change in the activity level of the muscle group studied.

Determination of maximal oxygen uptake. Twenty-one subjects had a single fatigue test as described. in addition, these subjects had a graded exercise test on a treadmill or bicycle ergometer to determine [VO.sub.2]max. Seven of the 21 subjects preferred running and were evaluated while running up a grade on a treadmill.([dagger]) Work rate was increased every 2 minutes until the subjects were unable to continue exercising by maintaining running position on the treadmill. The remainder of the subjects (n = 14) exercised on a cycle ergometer (Quinton Model 845([dagger])), Work rates were increased every 2 minutes by 150 kpm until the subjects were unable to continue exercising or maintain a pedal cadence of 60 rpm. Criteria for obtaining [VO.sub.2]max were a clear leveling off of oxygen uptake with an increase in work rate and respiratory exchange ratios greater than 1.15. During the last 3 to 4 minutes of each test, expired gases were collected in neoprene meteorological balloons at 30-second intervals. Fractions of oxygen and carbon dioxide in expired gases were analyzed with a mass spectrometer (Perkin-Elmer MGA 1100([dagger])), which was routinely calibrated with gases analyzed by the Scholander technique, and expired volumes were measured with a Tissot chaincompensated spirometer.

Data Analysis

The agreement in mean percentages of decline at the end of the fatigue test and at every 30-second interval during the 4 minutes of recovery on the initial test and retest were assessed using an intraclass correlation coefficient (ICC).[14] In addition, Pearson Product-Moment Correlation Coefficients were calculated to examine the relationships between [VO.sub.2]max and (1) the initial peak torque a 180[degrees]/s, (2) the percentage of decline in torque at the end of the fatigue test, and (3) the percentage of decline at 30 seconds of recovery.

Results

Test-retest reliability coefficients (ICCs) were high for percentage of torque decline at the end of the fatigue test and for each 30-second interval of recovery (Tab. 2). Peak torques at the beginning and end of the fatigue retest, as well as at every interval throughout recovery, were somewhat higher than the peak torque obtained during the initial test (Fig. 1), although the magnitude of the differences did not reach statistical significance.

[TABULAR DATA 2 OMITTED]

Recovery of muscle torque was rapid within the first 30- and 60-second intervals after the bout of fatiguing exercise, averaging 69% and 75% of initial torque range=46%-81%), respectively (Fig. 1). By the third and fourth minutes of recovery, muscle torque had recovered to within 90% to 95% of the initial torque output. Some subjects completely regained initial torque output, whereas complete muscle torque recovery in other individuals had not returned to initial torque levels until 10 minutes in recovery. As depicted in Figure 1, muscle torque recovery was nearly identical over a 5-day interval.

The mean and standard deviation of the [VO.sub.2]max values were 51 and 14.7 mL/kg/min, respectively, with a range of 30 to 76 mL/kg/min. Some individuals had very high levels of aerobic capacity, presumably from current and previous years of regular endurance exercise training. Other individuals were not regularly active in endurance exercise activities and had moderate or low [VO.sub.2]max values.

The relationships between [VO.sub.2]max and percentage of decline in torque at 30 seconds of recovery, peak torque at the start of the fatigue test, and percentage of decline in torque at the end of the fatigue test are shown in Figure 2. In general, higher [VO.sub.2]max values predict lower percentages of decline at 30 seconds of recovery (Fig. 2, top). In contrast, [VO.sub.2]max values, as an indicator of endurance capacity, do not reflect the initial torque output at 180[degrees]/s or the percentage of decline in peak torque at the end of the fatigue test (Fig. 2, middle and bottom).

Discussion

Intraclass correlation coefficients for the recovery of peak torque on the initial test and the retest at similar times of the day were high, ranging from .87 at the first 30-second interval of recovery to .67 at 2 1/2 minutes of recovery. Initial peak torque at 180[degrees]/s and percentage of decline in torque were highly reproducible over a 5-day interval when the time of day and diet were strictly controlled and reproduced. As Thorstensson and Karlsson[3] initially described, we believe controlling joint excursions, standardizing the rate of torque output by pacing, and standardizing the number of muscle contractions performed all help to reduce the high variability encountered during volitional fatigue tests, regardless of the range of initial torque outputs. Reproducing testing conditions such as the time of day, as well as diet and timing of meals, was designed to limit the variability in initial peak torque values, and may account for the high ICC value of .98 Tab. 2).

The average percentage of decline in muscle torque at the end of the fatigue test for all of our subjects was 59%, with a range of 35% to 84%. Although the fatigue protocol was standardized according to the description by Thorstensson and Karlsson,[3] we found greater percentages of decline from initial torque outputs over the 1-minute bout of fatiguing exercise. Thorstensson and Karlsson studied a small, homogeneous group of active, college-age male subjects who had a very narrow range of initial torque outputs, with an average percentage of decline of 45%. The results in our study extend their findings to a more heterogeneous group of individuals with a considerably wider range of initial torque outputs and more variable percentages of decline in torque with fatigue. A wider range of initial strength peak torque) outputs is more commonly found in rehabilitation settings in patients recovering from primary or secondary muscle deficits.

Similar to the Thorstensson and Karlsson[3] protocol, we did not correct for gravity for the weight of the subjects' limb and the lever arm. We acknowledge that the lack of gravity correction may have given us slightly different absolute peak torque values (ie, an underestimation of true peak torque values); however, we presume the influence of gravity on the magnitude of peak torque is small and unlikely to change over a short (5-day) test-retest interval. The effect of not correcting for gravity on the calculations of percentages of decline in torque, however, cannot readily be discerned from our data. Similarly, fatigue and recovery indexes are subject to the exact underestimation of peak torque and therefore should not have altered our findings. Though not directly assessed, we believe the error due to the lack of gravity correction is negligible.

The rapid recovery of muscle torque found after fatiguing exercise in this study is consistent with the findings of previous investigators.[10-13,1-19] Kroll,[15] who sampled at 1-minute intervals during recovery, reported percentages of initial torque outputs during the first minute of recovery similar to those of our study. Previous investigators[6-18] have reported that some subjects required up to 10 minutes to achieve complete recovery of muscle torque output. For the majority of subjects we have studied, recovery to 90% to 95% of initial torque output occurs by the third and fourth minutes of recovery. Complete muscle torque recovery may take as long as 10 minutes or more, depending on the type of contraction performed.[16] The right portion of Figure 1 (ie, 4-10 minutes) depicts one of the subjects who continued performing single maximal knee extensions at every 30-second interval for 10 minutes of recovery during her initial test. Her recovery pattern was not yet fully complete 10 minutes after stopping the fatigue test.

A closer inspection of Figure 1 clearly shows a rapid recovery of peak torque over the first minute, whereas recovery of peak torque was slower from 1 to 4 minutes following completion of the exercise bout. The rapid, early component of muscle torque recovery and a slower, late component of muscle torque throughut our recovery found in this study are or agreement with the original observations of Lind[19] for recovery of force after repeated submaximal isometric contractions. Clarke and Stull[16,18] have confirmed a similar two-component recovery period for both isometric and isotonic maximal contractions of the upper-extremity muscles.

Correlations between the initial peak torque output at 180[degrees]/s and the percentage of decline in peak torque with [VO.sub.2]max were low, suggesting little relationship between a central measure of endurance capacity and initial muscle peak torque output and percentage of decline at the end of the test (Fig. 2, middle and bottom). The negative correlation coefficient for initial peak torque at 180[degrees]/s suggests an inverse relationship between maximal aerobic capacity and maximal peak torque output and confirms our clinical observation that maximal peak torque may be lower (or may decline) in some individuals after high-intensity endurance exercise training.

We conducted an a posteriori analysis to determine whether subjects with higher initial peak torques had more decline or a steeper rate of decline. The average percentage of decline in torque at the end of the fatigue test for all subjects was 59%, with a range of 35% to 84% of the initial torque output. The percentage of decline in torque at the end of the fatigue test did not differ in individual subjects with high initial torque outputs (maximal peak [torque.sub.180[degrees]/s [greater than or equal to]90 ft[multiplied by]1b) compared with individuals with lower initial torque outputs (maximal peak [torque.sub.18[degrees]/s<70 ft[multiplied by]1b), suggesting the percentage of decline at the end of this fatigue test is not dependent on absolute level of initial torque output (data not shown). Similarly, a posteriori comparison of the percentages of decline at 30 seconds of recovery in an initial high torque output group with values obtained in an initial low torque output group demonstrated no significant differences, therefore no dependence on the level of absolute torque output.

As depicted in Figure 2 (top), the recovery of muscle torque at 30 seconds was strongly correlated with [VO.sub.2]max. This finding may be interpreted as suggesting that early recovery of muscle torque is a good predictor of local endurance exercise induced adaptations. Previously described fatigue tests have not been able to discriminate local muscle adaptations, in part due to the lack of standardization and high variability in percentages of decline with repeated contractions. The recovery of muscle peak torque after a standardized bout of fatiguing exercise appears to reflect differences in local muscle endurance capacity, irrespective of the level of initial torque output or extent of force decline. Recently, we have confirmed that the recovery of local muscle peak torque correlates well with training- and detraining-induced changes of the quadriceps femoris muscle.[20]

Because the recovery of muscle peak torque (recovery index) is reproducible and is able to discriminate presumed physiological adaptations in the quadriceps femoris muscle, we suggest this index be routinely included in the assessment of local muscle performance. Unlike Thorstensson and Karlsson's fatigue index,[3] we believe recovery indexes may reflect enhanced skeletal muscle respiratory capacity resulting from endurance types of exercise training. Recovery of peak torque after a standardized 1-minute bout of fatiguing exercise may better reflect the theoretical construct of muscle endurance capacity resulting from exercise or disease.

In addition to pointing out what we consider several measurement shortfalls, the results of this study bring into question the conceptual basis of the percentage- or rate-of-decline types of measures as an operational definition of local muscle fatigue. With the exception of sporting events that require anaerobic bursts of maximal activity, we would argue that there are few activities in life that mimic percent-of-decline types of fatigue tests. In contrast, individuals commonly exert themselves to a high capacity, rest, and then return to high-level activities (eg, heavy-material handlers). We believe recovery of muscle torque may reflect the endurance capacity of a group of muscles in individuals engaged in select occupations; however, further study is necessary confirm our assertion.

As stated previously, we acknowledge that the recovery of muscle peak torque assesses different metabolic pathways, as well as involves different physiological mechanisms as compared with rate-of-decline tests. Such a disparity in what each measure represents may also support greater ecological (ie, real-life) validity for the rate-of-recovery tests as opposed to the rate-of-decline tests. Additional studies are needed to determine whether recovery indexes are valid measures of local muscle endurance.

Conclusion

We seriously question the usefulness of two common clinically used tests of voluntary muscle fatigue, in part due to both theoretical and methodological flaws. We believe volitional tests of muscle fatigue should standardize methods to limit variability in dependent measures and control for factors known to influence muscle fatigue. Clinicians should consider utilizing objective measures of muscle fatigue that reflect adaptive changes in the muscle attributable to exercise or disease.

The recovery of muscle peak torque after a standardized 1-minute bout of dynamic isokinetic movements appears to be a reproducible, adjunctive measure for the assessment local muscle performance, which can reflect local muscle adaptations induced by aerobic exercise.

References

[1] Binder-Macleod SA, Snyder-Mackler L. Muscle fatigue: clinical implications for fatigue assessment and neuromuscular electrical stimulation. Phys Ther. 1993;73:902-910. [2] Holloszy JO, Booth FW. Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol. 1976;38:273-291. [3] Thorstensson A, Karisson J. Fatiguability and fibre composition of human skeletal muscle. Acta Physiol Scand. 1976;98:318-322. [4] Isolated Joint Testing and Exercise: A Handbook for Using Cybex[R] II. Ronkonkoma, NY: Cybex, Div of Lumex Inc; 1980:29, [5] Davies GJ. A Compendium of Isokinetics in Clinical Usage and Rehabilitation Techniques. 2nd ed. La Crosse, Wis: S & S Publishers; 1984: 27-36. [6] Winters DA, Wells RP, Orr GW. Errors in the use of isokinetic dynamometers. Eur J Appl Physiol. 1981;46:397-408. [7] Tesch P. Muscle fatigue in man with special reference to lactate accumulation during short-term intense exercise. Acta Physiol Scand suppl. 1980;480:1-40. [8] Tesch PA, Wright JE. Recovery from short-term intense exercise: its relation to capillary supply and blood lactate concentration. Eur J Appl Physiol 1983;52:98-103. [9] Jansson E, Dudley GA, Norman B, Tesch PA, Relationship of recovery from intense exercise to the oxidative potential of skeletal muscle. Acta Physiol Scand, 1990;139:147-152. [10] Sahlin K, Ren JM. Relationship of contraction capacity to metabolic changes during recovery from a fatiguing contraction. J Appl Physiol. 1989;67:648-654. [11] Harris RC, Edwards RHT, Hultman E, et al. The time course of phosphorylcreatine resynthesis during recovery of the quadriceps muscle in man. Pflugers Arch. 1976;367:137-142. [12] Sahlin K, Harris RC, Nylund B, et al. Lactate content and pH in muscle samples obtained after dynamic exercise. Pflugers Arch. 1976; 367:143-149, [13] Tesch PA, Thorsson A, Fujitsuka N. Creatinine phosphate in fiber types of skeletal muscle before and after exhaustive exercise. J Appl Physiol. 1989;66:1756-1759. [14] Lahey MA, Downey RG, Saal FE. Intraclass correlations: there's more than meets the eye. Psychol Bull. 1983;93:586-595. [15] Kroll W. Recovery patterns after local muscular fatigue for different levels of isometric strength. Int Z Angew Physiol. 1967;23:331-339. [16] Clarke DH, Stull GA. Strength recovery patterns following isometric and isotonic exercise. J Motor Behav. 1969;1:233-243, [17] Clarke DH. Strength recovery patterns from static and dynamic muscular fatigue. Research Quarterly. 1962;33:349-355. [18] Stull GA, Clarke DH. Patterns of recovery from following isometric and isotonic strength decrement. Med Sci Sports. 1971;3:135-139. [19] Lind AR. Muscle fatigue and recovery from fatigue induced by sustained contractions. J Physiol (Lond). 1959;127:162-171. [20] Sinacore DR, Coyle EF, Hagberg JM, Holloszy JO. Histochemical and physiological correlates of training- and detraining-induced changes in the recovery from a fatigue test. Phys Ther. 1993;73:661-667.

Invited Commentary

The article by Sinacore et al shows that peak torque, percentage of decline in peak torque at the end of a fatigue test, and percentage of decline in peak torque measured every 30 seconds during the recovery period following a fatigue test can be reliably measured in a population of healthy subjects. In addition, these data show that the percentage of decline in peak force measured 30 seconds after completion of a fatigue test (recovery index) is more highly correlated with the maximum aerobic capacity ([VO.sub.2]max) than either peak torque or percentage of decline in peak torque at the end of a fatigue test. Based on these observations, the authors state, "Recovery of peak torque after a standardized 1-minute bout of fatiguing exercise may better [than a fatigue index] reflect the theoretical construct of muscle endurance capacity resulting from exercise or disease." They also suggest that because fatigue indexes are insensitive to the physiological adaptations that are associated with changes in the fatiguability of a muscle, these indexes may not be valid measures of muscle endurance.

I disagree with the argument that the recovery index is a better tool for measuring muscle endurance, Muscle endurance is the complement of muscle fatigue. Muscle fatigue can be defined as a decrease in the force-generating ability of a muscle resulting from recent activation.[1,2] Fatigue may result from failure anywhere along the pathway involved in muscle activation, from the central nervous system to crossbridge cycling within the muscle.[3,4] Though a number of sites may be simultaneously contributing to the loss in the force-generating ability of a muscle during any functional activity or test, one site may be primarily responsible for the loss of force. The specific fatigue test used not only affects the amount and rate of fatigue, but also may determine the specific mechanisms that are responsible for the fatigue.[5] Different tests stress different sites within a muscle. Virtually all clinical fatigue tests primarily stress glycolytic pathways.[5] Thus, it should not be surprising that changes in the oxidative pathways of a muscle are not revealed by these tests. That none of these tests stress oxidative pathways does not make them invalid. We do not know whether it is limitations in the glycolytic or oxidative pathways that limit the performance of many patients. We cannot, therefore, determine the superiority of either the fatigue or recovery tests in assessing the function of a muscle.

Furthermore, though the outlined recovery index may ultimately prove to be a valuable clinical tool, I believe that the evidence presented does not support this conclusion. First, the authors state that the strong correlation between [VO.sub.2]max and "recovery of muscle torque at 30 seconds" may be interpreted to suggest that early recovery of muscle torque is a good predictor of "local endurance exercise-induced adaptations." This statement suggests that [VO.sub.2]max is a good predictor of local muscle endurance. If this is true, why not simply use the [VO.sub.2]max as the measurement of local muscle endurance? The reason, I believe, is that, as noted by the authors, [VO.sub.2]max is a measure of maximum acrobic capacity and not a measure of the endurance capacity of any specific muscle, Conclusions regarding the endurance of any particular muscle cannot be based on the [VO.sub.2]max of a subject. The correlation between [VO.sub.2]max and the recovery index, therefore, provides little evidence for the validity of the recovery index to assess the endurance ability of a muscle. In addition, the suggestion that the recovery index can measure a muscle's adaptation to endurance training is not based on the current data. This study did not measure changes (adaptation) in performance. Rather, the study compared peak torques with the subjects' current [VO.sub.2]max. Although the recovery index may correlate with adaptive changes in muscle histochemistry,[6] this was not tested. I therefore believe the validity of this measure for assessing muscle endurance is yet to be proven.

Finally, I question the generalizability of the results of this study to specific patient populations. The recovery index appears to be a reliable measure within a population of nondisabled young subjects. The proposed test, as is true for all volitional fatigue tests, appears to be an inappropriate test to use to measure local changes within a muscle if the patient either is not well motivated or has a disorder that affects the central drive to the muscle (eg, a cerebrovascular accident or parkinsonism). An alternative procedure is the use of an electrically elicited fatigue test.[5,7] These tests could easily be modified to allow for the calculation of a recovery index. The advantage of a test that uses electrical stimulation to produce and measure fatigue is that it localizes the site of fatigue to the peripheral components of the motor system and does not require central nervous system involvement.

In summary, I believe that more work is needed to prove the clinical validity of a recovery index for measuring muscle performance.

Stuart A Binder-Macleod, PhD, PT Associate Professor Department of Physical Therapy University of Delaware 315 McKinly Laboratory Newark, DE 19716

References

[1] Bigland-Ritchie B, Woods JJ. Changes in muscle contractile properties and neural control during muscular fatigue. Muscle Nerve. 1984:7:691-699. [2] Vollstad NK, Sejersted OM. Biochemical correlates of fatigue: a brief review. Eur J Appl Physiol 1988;57:336-347. [3] Clamann HP. Fatigue mechanisms and contractile changes in motor units of the cat hindlimb. Can J Spt Sci. 1987;12(suppl):205-255. [4] Westerblad H, Lee JA, Laennergren J, Allen DG. Cellular mechanisms of fatigue in skeletal muscle. Am J Physiol. 1991;261:C195-C209. [5] Binder-Macleod SA, Snyder-Mackler L. Muscle fatigue: clinical implications for fatigue assessment and neuromuscular electrical stimulation. Phys Ther, 1993;73:902-910. [6] Sinacore DR, Coyle EF, Hagberg JM, Holloszy JO. Histochemical and physiological correlates of training- and detraining-induced changes in the recovery from a fatigue test. Phys Ther. 1993;73:661-667. [7] McDonnell MK, Delitto A, Sinacore DR, Rose S. Electrically elicited fatigue test of the quadriceps femoris muscle. Phys Ther. 1987;67:941-946.

Author Response

Dr Binder-Macleod disagrees with our assertion that a recovery index following a standardized bout of fatiguing exercise is more reflective of local skeletal muscle endurance than is (1) the initial peak torque, (2) the decline in peak torque, or (3) the final peak torque. Dr Binder-Macleod appears to hold a traditional view of the clinical assessment of muscle fatigue (ie, focusing on decline in force), which we are challenging on both theoretical and methodological grounds. We maintain percentage-of-decline types of fatigue measures, though clinically used, have not been validated. We believe the recovery after fatiguing exercise not only has favorable measurement characteristics, but detects changes in muscle endurance capacity. Not only is recovery of muscle torque a reliable measure of local muscle endurance, but we maintain it is a responsive measure of muscle endurance in a healthy group of subjects. Jette[1] has described the responsiveness of a measure as its ability to detect clinically meaningful change. In a previous report, Sinacore et al[2] provided direct evidence that recovery of muscle torque is a better indicator (ie, more responsive measure) of endurance exercise training and detraining-induced adaptations than percentage-of-decline types of fatigue measures.

Though muscle endurance and muscle fatigue may be complementary, as Dr Binder-Macleod states, the metabolic events should not be construed as being physiologically similar or merely reciprocal events. Analogous to the metabolic events and regulation of glycogen synthesis and glycogen breakdown in skeletal muscle, these processes may be complementary, but they are markedly different, involving distinct enzymatic reactions, metabolic pathways, and time courses for maximal effects. Similarly, the decline in volitional peak torque from short-duration exercise may involve markedly different factors than the recovery of peak torque. We believe recovery indexes exploit these differences and capture meaningful changes in the endurance capacity of the quadriceps femoris muscle.

Dr Binder-Macleod is not surprised by the fact that current fatigue tests do not capture adaptations in oxidative capacity of skeletal muscles, because current fatigue protocols are stressing predominantly glycolytic pathways. We do not argue that repeated maximal voluntary exercise of 1-minute duration, as described, is predominantly a test of the ability to mobilize and use immediate sources of fuel (ie, high-energy phosphates) through depletion of endogenous stores and anaerobic glycolysis. There is substantial evidence that short-duration, maximal voluntary fatigue tests predominantly stress glycolytic pathways.[3] Our contention is that recovery of muscle torque reflects local muscle endurance capacity more than percentage-of-decline types of clinically used fatigue tests because a major adaptive response to endurance exercise training is an enhanced oxidative capacity. We do not mean to imply that the rate or extent of decline in muscle peak torque is not a valid measure of any biological phenomena. On the contrary, as Thorstensson and Karlsson[4] demonstrated, the percentage of decline may, in part, reflect the distribution of type II muscle fibers in the quadriceps femoris muscle. it must be emphasized that these are markedly different uses than most clinicians commonly have for such fatigue tests. Most clinicians would like a measure that demonstrates responses to adaptations from either exercise or disease.

There is a growing body of evidence that suggests the enhanced oxidative capacity of skeletal muscle is related to the recovery from short-term intense exercise.[5,6] it has been proposed that the level of oxidative enzymes of the tricarboxylic acid (FCA) cycle help restore high energy phosphates (ie, adenosine triphosphate and PCr) depleted by fatiguing exercise.[5,6] The enhanced oxidative capacity could be expected in both major types of skeletal muscle, particularly type I (slow-twitch) and type IIa (fast-twitch, oxidative-glycolytic) muscle fibers. A major adaptation to endurance exercise training and detraining is an increase and a decrease, respectively, in oxidative enzymes of the TCA cycle in type I and type IIa muscle fibers.[7] We contend that recovery indexes better reflect these local muscle endurance capacities than percentage-of-decline types of fatigue tests.

The reason we selected maximal oxygen uptake ([VO.sub.2]max) as our criterion measure was that it was readily obtainable, yet reflective of quadriceps femoris muscle endurance capacity. Because the quadriceps femoris muscle is a relatively large muscle mass involved in the generation of [VO.sub.2]max during bicycle ergometry or treadmill running, we were confident that recovery of quadriceps femoris muscle torque would be represented in and contribute to maximal aerobic capacity ([VO.sub.2]max). We could have readily selected other traditional measures that have been used to reflect local muscle endurance capacity such as mitochondrial volume, capillary density, oxidative enzymes of the TCA cycle, or changes in subpopulations of the type 11 muscle fiber pool as criterion measures; however, much more invasive procedures, such as muscle biopsies, would have been necessary in order to obtain these measures. Dr Binder-Macleod may have misinterpreted our rationale for selecting and using [VO.sub.2]max as our criterion measure. We did not attempt to imply nor do we believe that whole-body [VO.sub.2]max is likely to predict the muscle endurance capacity of every isolated skeletal muscle or small groups of skeletal muscles. Rather, [VO.sub.2]max is itself a reliable and responsive measure of the ability to utilize oxygen in large groups of aerobically working muscles such as the quadriceps femoris muscle. The homeostatic restoration of high-energy phosphates depleted from anaerobically working skeletal muscle appears to be, in part, an oxygen-dependent process involving the same oxidative enzymes of the energy transfer system used when the muscle is working aerobically.[5,6]

Dr Binder-Macleod questions the generalizability of our results to specific patient populations. Because recovery indexes are obtained from maximal voluntary efforts after maximal, fatiguing short-term exercise, they may be limited to well-motivated patients without disorders affecting the "central drive to the muscle." These limitations are the exact limitations of existing clinical tests of muscle fatigue. Recovery indexes are no substitute for sound clinical judgment, and we feel it is important that clinicians thoroughly understand appropriate tests and measures that are likely to reflect adaptations in skeletal muscles due to chronic neurological disorders (eg, cerebrovascular accident, multiple sclerosis, parkinsonism). We are not aware of any clinical tests of muscle fatigue that have been validated in patients with these types of chronic neurological disorders.

Dr Binder-Macleod further suggests that electrically elicited fatigue tests could readily be adapted as an alternative to maximal volitional fatigue tests (including recovery indexes) to localize fatigue to the peripheral components of the motor system because such tests do not require central nervous system involvement. This alternative has not been validated in individuals with central nervous system involvement. Furthermore, electrically elicited fatigue tests appear to be markedly different than volitional types of fatigue tests, particularly in the order of activation of skeletal muscle fibers as well as in the firing rates and synchrony of nerve depolarizations.[8]

Based on theoretical alternatives such as Dr Binder-Macleod has proposed, we recently investigated an electrically elicited fatigue test after 12 weeks of intense endurance exercise training in a group of nondisabled subjects. Though torque decline during an electrically elicited fatigue test appears to be a reliable measure,[9] the rate and extent of torque decline throughout the fatigue test is not sufficiently responsive for detecting meaningful changes in quadriceps femoris muscle endurance induced by intense exercise training (unpublished observations). Our observations underscore the need for more systematic investigations before theoretical alternatives are indiscriminately adapted for clinical use. The assessment of muscle fatigue using electrically elicited fatigue tests is an intriguing topic, but its discussion should be reserved for another report and commentary (perhaps by Dr Binder-Macleod), which we look forward to with great enthusiasm.

Finally, Dr Binder-Macleod states the validity of the recovery index has yet to be proven and further investigation is necessary. We concur with his latter sentiment; however, we believe our report offers a clinically meaningful assessment of muscle endurance heretofore not considered.

We appreciate the healthy skepticism Dr Binder-Macleod has taken of our report, and we are grateful for the opportunity to respond to his thoughtful criticisms. It is only through skepticism, careful scrutiny, and systematic investigation followed by meaningful discussion that we can document our clinical practice, including developing new assessment techniques. (*) Cybex, Div of Lumex Inc, 2100 Smithtown Ave, Ronkonkoma, NY 11779.

References

[1] Jette AM. Health-related quality of life measures in physical therapy outcomes research. Phys Ther. 1993;73:528-537. [2] Sinacore DR, Coyle EF, Hagberg JM, Holloszy JO. Histochemical and physiological correlates of training- and detraining-induced changes in the recovery from a fatigue test. Phys Ther. 1993;73:661-667. [3] McArdle WD, Katch FI, Katch VL. Exercise Physiology: Energy, Nutrition, and Human Performance. 3rd ed. Philadelphia, Pa: Lea & Febiger; 1991:206-207. [4] Thorstensson A, Karlsson J. Fatiguability and fibre composition of human skeletal muscle. Acta Physiol Scand. 1976;98:318-322. [5] Jansson E, Dudley GA, Norman B, Tesch PA. Relationship of recovery from intense exercise to the oxidative potential of skeletal muscle. Acta Physiol Scand 1990;139:147-152. [6] Tesch PA, Thorsson A, Fujitsuka N. Creatine phosphate in fiber types of skeletal muscle before and after exhaustive exercise. J Appl Physiol 1989;66:1756-1759. [7] Holloszy JO, Booth FW. Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol. 1976;38:273-291. [8] Delitto A, Snyder-Mackler L. Two theories of muscle strength augmentation using percutaneous electrical stimulation. Phys Ther. 1990; 70:158-164. [9] McDonnell MK, Delitto A, Sinacore DR, Rose SJ. Electrically elicited fatigue tests of the quadriceps femoris muscle: description and reliability. Phys Ther. 1987;67:941-945.

DR Sinacore, PhD, PT, is Assistant Professor, Program in Physical Therapy, Irene Walter Johnson Rehabilitation Research Institute, Washington University School of Medicine, Box 8502, 660 S Euclid Ave, St Louis, MO 63110 (USA). Address all correspondence to Dr Sinacore.

BL Bander, PT, is Chief of Physical Therapy, St John's Mercy Medical Center, 615 S New Ballas Rd, St Louis, MO 63141.

A Delitto, PhD, PT, is Assistant Professor, Department of Physical Therapy, School of Health and Rehabilitation Sciences, University of Pittsburgh Medical Center, 101 Pennsylvania Hall, Pittsburgh, PA 15261.

This study was approved by the Washington University School of Medicine Human Subjects Committee.

This article was submitted April 19, 1993, and was accepted September 13, 1993.