Time domain analysis. Rationale. For the respiratory muscles, as for any other skeletal muscles, a nearly linear relationship may be found between the pressure and the electrical activity they generate. The slope is related to force and the length of the diaphragm. As a result, for a given muscle length, a decrease in the ratio of respiratory muscle pressure to the integrated electromyographic activity of the muscle generating that pressure should, in theory, indicate a decrease in muscle contractility and the development of fatigue. Furthermore, it has been suggested that a decrease in this ratio indicates an alteration in excitation-contraction coupling (50). This point is also discussed in inferring Diaphragm Activation and Electromechanical Effectiveness from EMG in Section 6 of this Statement.

Methodology. The methodology required for electromyographic assessment is reviewed in detail in EMG Equipment and Data Analysis in Section 3 of this Statement.

Advantages. in theory, this is a useful approach for separating changes in pressure-generating capacity caused by neural or neuromuscular transmission factors from changes caused by peripheral muscular factors (51). One potential major advantage of this test is the possibility to detect fatigue during spontaneous breathing (52), because no special efforts are required by patients.

Disadvantages. For this index to be valid, other factors affecting respiratory muscle contractility, such as muscle length, chest wall configuration, or lung volume, should be controlled or kept constant (53). The applicability of this particular method to the respiratory system is limited by the difficulty of recording the activity of all the muscles involved in normal or augmented breathing that contribute to the measured pressure. Their relative contribution to the generated pressure is known to change during fatigue development (6, 28), and a reliable recording of the activity of a selective respiratory muscle group is regarded as difficult by some (54). Section 3 of this Statement offers a more optimistic view. in practice, the diaphragm, the neck accessory muscles, and the abdominal muscles are most amenable to this form of testing because their electrical activity can be more easily recorded without interference from other muscles and their force production (sternomastoid) or pressure output (diaphragm and abdominals) can also be recorded in relative isolation.

When interpreting results, one must also recognize that the relationships between integrated EMG activity of the respiratory muscles and the pressure they generate may not be perfectly linear (49).

if special precautions are not taken, EMG signals (particularly those recorded from the diaphragm with an esophageal electrode) can be subject to artifactual changes caused by variations in lung volume or chest wall configuration (55). Luckily, reports provide techniques that exclude many of the artifacts associated with esophageal diaphragmatic recording. Specifically, work by Sinderby, Grassino, and others provides a means of recording and analyzing electromyographic signals so as to exclude electrocardiogram (ECG), electrode motion, noise, and esophageal peristalsis artifacts (56-59). This latter work has also shown that it is possible, by using a multielectrode array, to reliably measure the diaphragm EMG amplitude and power spectrum in such a way that these variables are not affected by chest wall configuration and/or diaphragm length (56). Note, however, that even if EMG activity can be accurately recorded respiratory muscle pressures must also be reliably assessed for the pressure-to-integrated EMG ratio to be meaningful.

Applications. The theoretical value of time domain electromyo-graphic assessment in patients is that it can provide a means of determining whether observed reductions in respiratory muscle pressure-generating capacity are due to alterations in action potential transmission or to intrinsic alterations in peripheral muscle function (i.e., alterations in excitation-contraction coupling or contractile protein myofilament function). Although this technique is principally of value for experimental applications at the present time, ongoing efforts are being made to improve the reliability of this form of testing, and this type of measurement may assume a broader clinical role in the future.

Frequency domain analysis. Rationale. Frequency domain analysis of EMG signals from the respiratory muscles has been proposed as a test to detect the occurrence of respiratory muscle fatigue in humans (60), because the power spectrum of skin surface-recorded EMG signals typically shifts to lower frequencies during fatiguing contractions (see Figure 4).

Several indices of the power spectrum have been used for this purpose, including an assessment of the "center" or "cen-troid" frequency of the power spectrum and a "power ratio" of a high-frequency band over a low-frequency one. Both of these indices appear to decrease with fatigue and increase with recovery. With appropriate instrumentation, these analyses can be obtained "on line" in spontaneously breathing subjects or patients. Shifts in the EMG power spectrum indicative of diaphragmatic fatigue have been documented during severe whole body exercise (61) and during loaded breathing in normal subjects, in female patients during delivery (39), as well as in ventilator-dependent patients having weaning problems (2).

Methodology. The methodology required for electromyo-graphic assessment is reviewed in detail in EMG Equipment and Data Analysis in Section 3 of this Statement.

Advantages. Studies of normal subjects have shown a good correlation between EMG power spectrum shifts and force or pressure losses at high stimulation frequencies (high-frequency fatigue) but not with force loss at low stimulation frequencies (low-frequency fatigue) (62). High-frequency fatigue is typically associated with failure at the neuromuscular junction or at the sarcolemma. in line with these predictions, a good correspondence has been found for the human diaphragm between the rate of power spectrum shift, the pressure-time product (63), and the changes of the shape of the action potential wave form measured during phrenic nerve stimulation.

Disadvantages. The etiology of power spectral shifts with fatigue is still controversial. Possible mechanisms include a slowing of muscle fiber conduction velocity, a widening of the action potential waveform, a decrease in motor unit discharge rate, or synchronization of motor units firing (64). None of these can be directly linked to a fatiguing process at the sarco-mere level. Power spectrum shifts are therefore related to central motor control, or reflex pathways, or changes in electrolyte or metabolite concentrations within the muscles.

in addition, power spectrum shifts are rapidly reversed on rest or with reduced activity even though the muscle may remain in a fatigued state. Power spectrum analysis of an EMG,

Figure 4. Time course of various parameters during an isometric contraction held at 40% of maximal force (task) until failure. From the top: Maximal force: voluntary maximal electrical supramaximal pulses of the nerve. The vertical lines are pressure swings obtained by electrical stimulation, showing a progressive loss of maximal force. The time elapsed from the start until task failure is known as the time limit, or endurance. The exercise is defined as a fatiguing task, because there was loss of maximal force. Regaining the ability to develop maximal force takes a few minutes. Regaining the ability to perform the same task again, however, takes hours. This panel shows the time course of the central frequency (CF) of the EMG obtained via surface electrodes and fast Fourier transforms in the same exercise. Decay of CF is fast, and is a forewarning of task failure. This parameter is an expression of membrane potential conduction velocity. Relaxation rate: The time course of relaxation time (if the contraction is interrupted). Control values are the same as in a rested muscle. This parameter is linked to failure at the sarcomere level, mainly related to calcium coupling and release from troponin. Tetanic force: The decrease in force during an electrical stimulation at 100 or 20 Hz, and its ensuing rate of recovery. Recovery from fatigue is faster when the muscle is probed with 100 Hz than with 20 Hz; the former is proposed to be caused by conduction mechanisms, whereas the latter is mediated by contraction mechanisms. Spontaneous shortening: Spontaneous shortening of the diaphragm before (100%) and after task failure, and time of recovery. Figure used by permission from Dr. A. E. Grassino.

therefore, cannot provide an indication as to the state of the contractile system or the excitation-contraction coupling process, or how these may change with fatigue. As mentioned previously, because of the close association of these indices with neural or sarcolemmal events, power spectral shifts recover quickly with rest (within 5 minutes). As a result, these indices can be markedly affected by the breathing pattern (63) and the breathing strategy employed (29), which in turn may cause a high breath-to-breath variability.

Applications. Because of the problems listed above, this test cannot be taken as a reliable global index of the development of muscle fatigue. The principal utility of this test is that demonstration of an EMG spectral power shift in a working muscle may provide some clue to the development of an alteration in neuromuscular transmission.

Muscle Responses to External Stimulation

Pressure-frequency relationships. Rationale. Fatigue, defined as a decrease in the pressure- or force-generating capacity of a muscle under loaded conditions, can be most specifically detected by recording the pressure- or force-frequency curve of that muscle in response to artificial motor nerve stimulation. Of the respiratory muscles, the diaphragm (16, 65) and the sternomastoid (66) muscles are most amenable to this form of testing. Low-frequency fatigue has been documented for these muscles in normal subjects during loaded breathing (16) as well as during intense exercise (67).

Methodology. The methodology required for phrenic nerve stimulation and sternomastoid stimulation is reviewed in detail in Section 2 of this Statement.

Advantages. This technique overcomes many of the difficulties associated with volitional or spontaneous breathing efforts. Indeed, the responses are not complicated by possible variations in the level of effort expended. The response of a particular muscle can also be studied in isolation, free from the activity of other muscles. Changes in the shape of the pressure- or force-frequency curves also give indications as to the underlying mechanism of fatigue. For example, a decreased pressure or force at high stimulation frequencies may be indicative of impairment at the neuromuscular junction or at the sarcolemma, whereas a decreased force or pressure at low stimulation frequencies may suggest a possible impairment of excitation-contraction coupling.

Disadvantages. This is a difficult test to perform. Tetanic stimulation can also be painful and it may be necessary to anesthetize the skin near the electrodes. To overcome this problem, partial pressure-frequency curves may be constructed by using twin pulses and by varying the intervals between the pulses (68, 69). These are better tolerated than tetanic stimulation and can provide comparable information regarding the presence of high- and low-frequency fatigue. Because of a large intersubject variability in the responses to artificial stimulation, fatigue can be reliably detected by these techniques only when a subject serves as his/her own control. A possible exception concerns the ratio of the force or pressure developed at a low stimulation frequency (i.e., 20 Hz) over that at a high stimulation frequency (i.e., 100 Hz), for which some critical value may be recognized below which low-frequency fatigue may be said to be present (16, 65, 66, 68).

Application. Although this test provides a means of directly detecting the development of muscle fatigue, applicability of this approach is limited by (1) patient discomfort associated with high-frequency stimulation, (2) equipment expense and complexity, and (3) the need to carefully control for variation in body position, lung volume, and the electrode-nerve interface. Advances in magnetic stimulation techniques may allow a variation of this form of testing to reach more widespread clinical application in the future, but this test is currently limited to research applications.

Single twitch stimulation. Rationale. As an alternative to tetanic or twin pulse stimulation, recording of muscle twitches in response to single nerve shocks can be employed to detect the presence of low-frequency fatigue (68). Twitch responses are much easier to obtain but are more variable than tetanic responses and are subject to additional variations caused by phenomena such as twitch potentiation (70).

Methods and equipment. The methodology required for phrenic nerve stimulation is reviewed in Section 2 of this Statement.

Advantages. This technique is nonvolitional, eliminating concerns about patient effort in the interpretation of obtained results. In addition, because only single twitches are evoked when employing this technique, much less patient discomfort is involved when compared with that produced by construction of the force-frequency relationship. Because a single shock is, by definition, a "low-frequency" stimulus, this approach also pro vides a means of detecting the development of low-frequency fatigue, whereas measurement of maximal volitionally produced pressure does not. in addition, the magnitude of the compound action potential evoked during single twitches can be measured and monitored over time; correlation of this assessment with force generation over time may provide a means of detecting alterations in neuromuscular transmission.

Disadvantages. The application of these tests has been largely limited to scientific investigations in normal subjects and patients with lung (71) or neuromuscular diseases (72). Their application in clinical settings is more difficult, partly because of the factors already mentioned but also because of the many pieces of equipment that are required to perform these tests. in the case of the diaphragm, these difficulties are compounded by the necessity of stimulating the phrenic nerves bilaterally. in addition, it is critical that supramaximal-ity be attained during electrical stimulation for this test to be useful. unless electrical current is sufficiently high (i.e., increased to a level 150% of that required to initially attain a maximal signal), alterations in the compound action potential over time may simply reflect local, axonal changes. The introduction of magnetic stimulation (73) and of phonomyography (74) may help overcome some of these difficulties.

Applications. Although this technique holds promise, more work is needed before this test can be used in the clinical arena. Because of the technical problems detailed above, it is difficult to use present stimulation techniques to accurately evaluate the time course of fatigue, and this approach is currently better suited for evaluation of the effect of an intervention or treatment on muscle function. once standardization of this technique is achieved, it probably offers the greatest promise to provide an objective index of the development of muscle fatigue.

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