UNUSUAL TIREDNESS or fatigue is a common complaint
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1 770 Electrophysiologic Evaluation of Muscle Fatigue Development and Recovery in Late Polio Katharina Stibrant Sunnerhagen, MD, PhD, Ulrika Carlsson, MS, Arne Sandberg, MD, Erik Stålberg, MD, PhD, Marita Hedberg, Gunnar Grimby, MD, PhD ABSTRACT. Sunnerhagen KS, Carlsson U, Sandberg A, Stålberg E, Hedberg M, Grimby G. Electrophysiologic evaluation of muscle fatigue development and recovery in late polio. Arch Phys Med Rehabil 2000;81: Objectives: To study aspects of fatigue in late-polio patients and healthy controls. We hypothesized that late-polio subjects would develop more peripheral fatigue, assessed with surface electromyography (EMG), and that no major differences would exist between the two groups in neuromuscular junction transmission. Design: Case-control study. Setting: University hospital laboratory. Subjects: Ten patients with a history of polio (mean age, 54 yrs, SD 5; mean time since polio onset, 49 yrs, SD 7) and a matched control group (mean age, 52 yrs, SD 8). Methods: A protocol with a stepwise force increase up to 80% of maximal voluntary contraction ending with an 8-minute recovery period was performed twice, first with surface EMG and then with electrical stimulation and surface-recorded evoked M-response. Main Outcome Measures: Surface EMG analysis of voluntary activity and evoked M-response. Results: No significant differences existed between groups in the relative decrease during the fatigue protocol. The recovery of force was slower in the late-polio subjects. A reduction in the root mean square (RMS) value during recovery was seen in the polio group, although a normalization of the mean power frequency (MPF) was seen in both groups. Conclusion: The weakness during the fatigue procedure was not caused by neuromuscular blockade, because electrical nerve stimulation evoked a normal response. The weakness after exercise was the result of a slow recovery that may reflect both central and peripheral fatigue. Key Words: Electromyography; Muscle fatigue; Postpoliomyelitis syndrome; Rehabilitation by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation From the Department of Rehabilitation Medicine, Göteborg University, Göteborg (Sunnerhagen, Carlsson, Hedberg, Grimby), and the Department of Clinical Neurophysiology, Uppsala University, Uppsala (Sandberg, Stålberg), Sweden. Submitted June 21, Accepted in revised form November 5, Supported by the King Gustav V 80-Years Foundation and by a research stipend from the Swedish Medical Research Council (project GG, project 0135 ES). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Katharina Stibrant Sunnerhagen, Department of Rehabilitation Medicine, Sahlgrenska University Hospital, Guldhedsgatan 19, S Göteborg, Sweden /00/ $3.00/0 doi: /apmr UNUSUAL TIREDNESS or fatigue is a common complaint in late-polio subjects, who report new symptoms many years after the onset of disease. 1 Fatigue combined with new or increased muscular weakness and muscle and joint pain constitute the cardinal symptoms in the postpoliomyelitis syndrome. 2 According to Edwards, 3 muscular fatigue during isometric activity is defined as a failure to maintain the required or expected force. This fatigue may be from either central or peripheral performance elements. Central fatigue is a voluntary or involuntary failure of neural drive that reduces: (1) the number of functioning motor units, and (2) motor unit firing frequency. Peripheral fatigue is a failure of the muscles ability to generate force, either because of high-frequency fatigue caused by impaired neuromuscular transmission and failed muscle action potentials, or low-frequency fatigue caused by impaired excitation/contraction coupling. 3 Electromyographic (EMG) signal changes over time, expressed as root mean square (RMS), will mainly reflect changes of muscle activation including firing rate, number of active motor units, and size of their electrical signals. Reduction of RMS during maximal voluntary activation may indicate central fatigue. A progressive spectral compression of the EMG signal toward lower frequencies has been suggested to be related to peripheral fatigue during sustained contractions. 4 Thus, muscle fatigue can be studied by means of the mean power frequency (MPF). Muscles with a high percentage of fast-twitch fibers are suggested to decrease more in MPF than those with low fast-twitch fiber content. 5 Interest has been raised in the correlation between metabolic changes as measured with 31 P magnetic resonance spectroscopy (MRS) and changes in median power frequencies. 6,7 However, a recent study 8 showed no correlations in healthy subjects between metabolic changes as recorded with MRS and changes in median power frequencies. An interindividual variability occurred for changes in both myoelectrical and MRS. The perceived fatigue and decreased endurance found in patients with postpolio syndrome has no clear pathophysiologic explanation, 9-12 perhaps because of how fatigue is defined in relation to absolute or relative performance. Sharma and coworkers 13 suggested that impaired calcium kinetics plays a role in postpolio patients fatigue, drawing this conclusion from an absence of abnormal findings on MRS, but a significantly larger decline in voluntary maximal contraction and tetanic force 13 than in healthy subjects. Other factors may also be of importance. Biopsy studies have shown lower levels of oxidative enzymes in late-polio subjects. 14,15 Trojan and colleagues 16 reported defects in neuromuscular transmission in patients with postpolio fatigue, which led to trials with acetylcholinesterase inhibitors to reduce the development of fatigue. The aim of the present study was to study aspects of fatigue and subsequent recovery in late-polio subjects and in a healthy control group, using a progressive exercise model with continuous surface EMG recording.
2 ELECTROPHYSIOLOGY OF FATIGUE IN LATE POLIO, Sunnerhagen 771 Table 1: Data of the Polio Subjects Sex Age (yrs) Time Since Onset (yrs) MVC* (%) Median Macro EMG F F F F F M M M M M * Values are reported as % of normal. Amplitude times the control values reported by Stålberg and Trontelj. 17 MATERIALS AND METHODS Study Groups Ten patients (5 women, 5 men; mean age, 54yrs [SD 5]) with a history of polio averaging 49yrs (SD 7) since onset participated in the present study (table 1). All had documented clinical involvement in the tested limb. EMG confirmed the polio involvement. All except 1 patient had documented weakness of the anterior tibial muscle. Nine had markedly increased motor units, as shown by the very large median macro unit potential amplitudes (median, 6.2 times control values; range, 3-31), indicating a large degree of reinnervation; 17 The tenth had 1.8. The muscle strength for isometric ankle dorsiflexion measured with a Kin-Com dynamometer a was moderately reduced, with a median of 58% (range, 5-11, with only 1 subject above 77%) of predicted values. 18 The healthy control group consisted of 10 age- and sex-matched subjects, with a mean age of 52 years (SD 8). All participants gave informed consent to participate in the study according to the Declaration of Helsinki. The Ethics Committee of the Faculty of Medicine, Göteborg University, approved the study. Test Procedure The subject was in a supine position on a bench with the foot secured to the platform. All subjects wore standardized shoes. The room in which the test was performed was unlit and quiet so that the subject was able to concentrate during the test. For familiarization with the method, the subject performed 10 submaximal dorsiflexions at the 10% level. After a rest, the subject performed the test according to the test protocol with verbal encouragement. The subjects were tested twice, once with surface EMG analysis of voluntary activity and once with repetitive nerve stimulation and surface-recorded muscle response (M wave). The test protocol (fig 1) was as follows. The subject first performed an isometric ankle dorsiflexion with maximal voluntary effort two to three times to ensure that a maximal voluntary force was recorded. After a 2-minute rest, the subject performed 10 isometric dorsiflexions at a submaximal force level of 10% of the maximal voluntary contraction (MVC) to become familiar with the procedure. Each contraction lasted for 6 seconds, with a 4-second rest interval after each contraction. A maximal dorsiflexion was again performed immediately after this series. After a 10-second rest, another series of 10 dorsiflexions started at a force level of 20%, followed by a maximal voluntary dorsiflexion at the end. In this manner, the test continued with a 10% increase at every level until 80% of the maximal force was reached. During the recovery phase, a maximal dorsiflexion was performed after 2, 4, 6, and 8 minutes (fig 1). Equipment Set-up A specially developed force transducer b connected to a portable computer recorded force for ankle dorsiflexion. The transducer was connected to a platform placed at a 90 angle relative to the bench on which the subject was lying. The sole of the foot was against the platform, and a Velcro strap secured the foot (fig 2). When the foot of the subject was in dorsiflexion, the transducer measured the force that developed. Force levels above or below the preset target were indicated by a sound, thereby providing feedback so the subject could maintain an approximately constant force level. Surface EMG was recorded with Ag/AgCl surface electrode discs c with a diameter of 9mm. The subject s skin was shaved and scrubbed with alcohol, and two electrodes at a distance of approximately 30mm were secured to the belly of the anterior tibial muscle in a direction parallel to the tibia. The ground electrode was placed on a bony part of the knee. The EMG signal was preamplified with a gain of 1000, an input impedance of more than 0.5MOhm at 50Hz, a CMRR of more than 100dB, and a band width of Hz by a HDX 82 preamplifier. a The signal was bandpass-filtered between 7 and 490Hz. The EMG was sampled at a frequency of 1250Hz with an analogue input-board d on a Macintosh computer with software developed in Lab View. d,e The EMG signal was then Fig 1. Schematic model of the study protocol, each vertical bar representing an isometric ankle dorsiflexion. Shaded area: 10 dorsiflexions at 10% of the MVC for familiarization of the method. Arrows: repetitive stimulation of the peroneal nerve with simultaneous recording of the M wave over the anterior tibial muscle.
3 772 ELECTROPHYSIOLOGY OF FATIGUE IN LATE POLIO, Sunnerhagen immediately after the fatigue test. The force measured at maximal effort 2, 4, 6, and 8 minutes after the end of the fatigue test were compared with the values measured at maximal effort performed before the start of the fatigue test. Comparisons were made between the two groups. The RMS and MPF measured at maximal effort 8 minutes after the end of the fatigue test were compared with the values measured at maximal effort performed before the start of the fatigue test. The M waves evoked at repetitive nerve stimulation were measured automatically but with operator supervision. The following parameters were assessed: baseline-negative peak amplitude of the first response for each train, change in amplitude between the first and fourth response (so-called decrement) expressed as relative amplitude change of the fourth compared with the first M wave. Fig 2. Equipment set-up to record ankle dorsiflexion. The sole of the foot was placed toward the platform and a Velcro strap secured the foot. On the back of the platform a specially developed force transducer connected to a portable computer recorded force for ankle dorsiflexion. bandpass-filtered using a Butterworth filter with cut-off frequencies of 10 and 300Hz. To study the subject s response to electrical stimulation, recording surface electrodes were placed over the mid-portion of the anterior tibial muscle and distally over its tendon. The peroneal nerve was stimulated at the level of the fibula head. Stimulus strength was set to 125% of that giving maximal muscle response. The stimulus pulse duration was 0.1ms. The muscle responses at electrical stimulation (M waves) were recorded and analyzed with commercial EMG equipment. f The nerve was stimulated with trains of stimuli, consisting of 5 pulses at 3Hz. The following protocol was used: testing directly after the preparatory series of submaximal contractions, immediately after two short periods of MVC, before maximal contraction following submaximal levels of 50%, 70%, and 80%. During the recovery phase, tests were performed before the series of MVCs at 2, 4, and 6 minutes, and after the MVC at 8 minutes. Analysis For the analysis of the EMG, a time window was set at the middle part of each contraction. A time period of 0.84s was used (multiples of 0.42 are available) to ensure that enough information was present for the analysis and that a maximal effort had occurred during the contraction period. For each such part, the amplitude of the signal was expressed as the RMS. Fast Fourier transformation was used to obtain the MPF. The mean value of the 10 force values and the 10 RMS and MPF values, respectively, at each preset force level were calculated as the percentage of the value at the 10% level and were plotted for each individual. The percent changes of the values were then calculated using regression analysis for the force, RMS, and MPF values for each individual. The maximal values of force, RMS, and MPF after each submaximal level and during recovery were calculated as the percent of the values at the first maximal contraction. The percent changes from the first maximal contraction of the force and the RMS and MPF values were then calculated using regression analysis. This calculation was performed for each individual. The force, RMS values, and MPF values measured at maximal effort 2 minutes after the end of the fatigue test were compared with the values measured with maximal effort Statistics We used mean values and standard deviations in the description of the subjects. For results, values are presented as mean and standard error of the mean. We used the Wilcoxon one-sample nonparametric test to evaluate differences between paired observations and the Mann-Whitney U test for differences between groups. A significance level of p.05 was used. RESULTS Contraction With Maximal Effort The force at maximal voluntary contraction was 124N (s x 25N; median, 92; range, 40 to 292) for the late-polio group and 185N (s x 24; median, 166; range, 104 to 348) for the control group, with a significant difference of p.05. The maximal force decreased significantly ( p.005) during the fatigue protocol both for the late-polio group and the control group. The decrease was 45% (s x 7%) for the late-polio group and 37% (s x 3%) for the control group. No significant difference existed in the relative decrease between the two groups (fig 3). The force increased significantly ( p.01) 2 minutes after the end of the fatigue protocol for the control group (table 2). No such significant change was found for the polio group. Significant differences existed in the recovery pattern between the two groups. After 8 minutes of rest, neither the polio group nor the control group had regained their initial force values ( p.01). The RMS values at maximal effort during the fatigue protocol did not change significantly for either group. The RMS was significantly lower ( p.05) at the test 2 minutes directly after the end of the fatigue protocol for the late-polio group (4.8% 2%), while no significant difference from the end value was found for the control group (4.1% 4%). Eight minutes after the fatigue protocol, neither the late-polio group ( p.05) nor the control group ( p.01) reached the RMS values measured at maximal effort before the test (fig 3). The MPF decreased significantly during the fatigue protocol, with 10% (s x 4%, p.05) for the late-polio group and 13% (s x 2%, p.005) for the control group, with no significance between the two groups. Two minutes after the fatigue protocol, the MPF values for both the polio group and the control group increased significantly ( p.005) above the values at the end of the fatigue protocol. Eight minutes after the end of the fatigue protocol, both the polio group and the control group had reached the initial MPF values measured at maximal effort before the start of the fatigue protocol.
4 ELECTROPHYSIOLOGY OF FATIGUE IN LATE POLIO, Sunnerhagen 773 Fig 3. Values of force, MPF, and RMS during the fatigue protocol and the recovery period. Results at the Stepwise Increase in Contraction Force The target force increase was 800%. Neither group reached the increased target force. The actual force increase was 362% (s x 77%) for the polio group and 519% (s x 45%) for the control group, with no significant differences between the two groups (fig 4). The RMS increased significantly with increasing force levels by 135% (s x 31%, p.01) from the 10% force level for the late-polio group and by 299% in the control group (s x 60%, p.005), with a significant difference ( p.05) between the two groups (fig 4). The MPF did not change significantly during the submaximal contractions with increasing force levels for either of the two groups (fig 4). Table 2: Recovery Phase Values, Controls Versus Late-Polio Subjects Mean (%) Controls Md (%) p Polio Subjects Mean (%) Md (%) p Between-Group Differences (p) 2 minutes ns minutes ns ns 6 minutes ns 8 minutes ns Values are reported as mean standard error of the mean, and median. Abbreviations: Md, median; ns, not significant. Fig 4. Results at stepwise increase in contraction force. The RMS increased significantly with increasing force levels for both groups, less pronounced for the polio group. The MPF did not change significantly for either group. Electrical Stimulation Seventy-two recordings in eight controls and 75 recordings in nine polio subjects were of acceptable signal quality. The initial amplitudes varied between subjects, depending on muscle volume and recording conditions. However, the amplitude also varied within the test. The first two tests (ie, before MVC and after the second MVC before the fatigue phase) were performed for method evaluation. The intraindividual amplitude variation was the same in the controls (mean, 3.7%; s 3%) as in the polio subjects (mean, 4.7%; s 5.3%). In controls, the amplitudes had increased by 1.4% immediately after the last contraction in the fatigue test, compared with the initial control values. In late-polio subjects, the amplitude had decreased by 4.7%, but no significant difference was found between controls and patients (fig 5). No change was seen in the recovery phase. The decrement was 0.4% in controls (range, 3.5% to 3.5%) before the fatigue protocol. The decrement did not change during or after the fatigue protocol. The decrement was 0.9% (range, 10% to 6%) in the polio subjects with no change during or after the fatigue protocol. There was no difference in decrement, compared with the controls (fig 6).
5 774 ELECTROPHYSIOLOGY OF FATIGUE IN LATE POLIO, Sunnerhagen in motor unit parameters (change in shape and firing rate) are more directly reflected in RMS than in normal muscle. The central factors that influence firing rate and number of motor units can to some extent be studied directly from EMG recordings and from the method of intrapolated twitches during maximal effort. 19 Studies regarding central activation show conflicting results. Allen and associates 20,21 noted that the muscle activation in the elbow flexors in late-polio subjects at maximal voluntary effort was not complete in the unfatigued state or during fatiguing submaximal exercise. During fatiguing exercise, the muscles showed evidence of both central and peripheral fatigue. Grimby and coworkers 22 showed only a slight lack of activation in the quadriceps muscle. The degree of motor unit activation at maximal effort can, however, vary between different muscles in the same individual. Fig 5. Mean ( standard error) M-wave amplitude for the anterior tibial muscle at electrical stimulation of the peroneal nerve before, during, and after the fatigue test for controls and polio subjects. The M wave did not change during the test for either group. DISCUSSION In the present study, no significant differences were observed in electrophysiologic variables in the anterior tibial muscle between subjects with late polio and healthy controls during the fatigue protocol. However, the polio subjects showed a slower recovery of force. A further reduction in RMS value after the end of exercise was noted, but was not seen in controls. There was a recovery in MPF both in healthy controls and in late-polio subjects. How are these neurophysiologic findings related to the corresponding weakness that developed during the fatiguing test? Reduced RMS will mainly reflect changes of muscle activation including firing rate, number of active motor units, and size of their electrical signals. This muscle activation pattern is particularly evident in a muscle with few motor units, as after the reinnervation that occurs in late polio. Postpolio muscle has less so-called phase cancellation; therefore, changes Fig 6. Mean ( standard error) decrement of the M-wave amplitude for the anterior tibial muscle at repeated electrical stimulation (5 stim, 3Hz) of the peroneal nerve at the level of the fibula head, for controls and polio subjects. There is no change in the decrement during the test for either group.
6 ELECTROPHYSIOLOGY OF FATIGUE IN LATE POLIO, Sunnerhagen 775 Our results with a reduced RMS but normal MPF in the early recovery phase compared with controls may be explained by a reduced firing rate, and thus a central factor cannot be rule out. Another possible explanation in this context is the fact that the amplitude of active motor unit signals normally increases during submaximal fatiguing activity. The change in RMS value during fatiguing-muscle contraction therefore reflects a combination of factors, some reducing the amplitude (reduced firing rate) and some increasing the amplitude (membranedependent changes in signals shape). Immediately after a fatiguing activity, the amplitude of individual motor units returns to normal. If the firing rate recovers with a slower timescale, the effect of this parameter will be demasked. This difference in time scale among two opposing phenomena may result in a further reduction in RMS in early recovery phase, although it really means a faster recovery in one of the opposing factors determining RMS. A similar phenomenon of a change in the signal shape is seen in the MPF, with a reduction in frequencies during the test and recovery. The change in RMS value may be both central and peripheral, and may be interpreted either as a normalization of effects occurring during the fatigue protocol or as new fatigue phenomena during recovery. Because the effects in this study are also seen in healthy controls, they can probably not explain the slow recovery of force in late-polio subjects after the fatigue protocol. Rodriguez and Agre 23 also found that late-polio subjects have a different strength recovery curve than healthy persons, although the amplitude of the EMG in their study did not show differences between polio subjects and controls. They considered the delayed recovery process in the late-polio subjects to be caused by local muscle fatigue. This is in accord with the Sharma group s 13 findings explaining the muscle fatigue in the late-polio patients as impaired calcium kinetics. A reduced Ca 2 release may be a result of impaired action potential invasion in the T tubules, as shown by Westerblad and colleagues. 24 Trojan and coworkers 25 found a reduction in the compound motor action potential on repetitive stimulation in late-polio patients, which may be caused by a prolonged reduced membrane potential which in turn may be the result of a reduced potassium gradient. 26 In a subsequent study with MRS using the same group of subjects and the same fatigue protocol as the present study, we found reduced intramuscular ph in late-polio subjects, compared with healthy controls, during the first minutes after exercise. There were no significant differences in phosphorcreatinine or inorganic phosphorous during and after the fatiguing exercise (unpublished data). In the present study, electrical stimulation produced some variability in evoked muscle responses. This finding may be partly the result of technical errors, and may partly result from biological factors such as muscle shortening and temperature change after contractions. On one hand amplitude increase after short maximal contraction is a well-known normal phenomenon. 27 On the other hand, the slightly decrementing amplitudes, both in controls and in late-polio patients, are most likely technical. Because of method problems, the anterior tibial muscle is usually not used in diagnostic tests eg, in diagnosing myasthenia gravis. The most important findings of the present study are, however, that no significant differences existed between the late-polio patients and controls after stimulation in any of the variables. It is true that neuromuscular transmission is abnormal as shown by Trojan et al s 12 singlefiber EMG. If the degree of neuromuscular blocking had been of clinical significance, the decrement test also should have shown abnormality. Thus, our results indicate that the recorded fatigue is not localized to neuromuscular transmission and that the electrical event along the muscle fibers seems unchanged during and after the fatigue protocol used in the present study. These results are therefore in contrast to those of Trojan. 12 We found a slower immediate recovery during the first 2 minutes in the polio subjects compared with the control group. This agrees with other studies 13,22,23 that report slower recovery of force after exhausting exercise. The reduced recovery of MVCs may be attributable to central and/or peripheral factors in various combinations, probably to the type of fatiguing exercise. In the present study, successively increasing contraction levels to exhaustion were used, while other researchers used submaximal contractions. Peripheral factors such as muscle fibers contractility processes may be of greatest importance. We could not show that late-polio subjects fatigued during the exercise more than healthy controls using the same relative force levels. References 1. Cosgrove JL, Alexander MA, Kitts EL, Swan BE, Klein MJ, Bauer RE. Late effects of poliomyelitis. Arch Phys Med Rehabil 1987;68: Halstead L, Rossi C. Postpolio syndrome: clinical experience with 132 consecutive outpatients. In: Halstead LS, Weicher DO, editors. Research and clinical aspects of the late effects of poliomyelitis. New York: March of Dimes Birth Defects Foundation; p Edwards RHT. Human muscle function and fatigue. In: CIBA Foundation Symposium, vol 82. London: Pitman Medical; p Lindström L, Magnusson R, Petersén I. Muscular fatigue and action potential conduction velocity changes studied with frequency analysis of the EMG signals. Electromyography 1970;4: Komi P, Tesch P. EMG frequency spectrum, muscle structure and fatigue during dynamic contractions in man. Eur J Appl Physiol 1979;42: Zwarts M, Van Weerden T, Haenen H. Relationship between average muscle fiber conduction velocity and EMG power spectra during isometric contraction, recovery and applied ischemia. Eur J Appl Physiol 1987;56: Miller R, Boska M, Moussavi R, Carson P, Weiner M. 31-P nuclear magnetic resonance studies of high energy phosphates and ph in human muscle fatigue. J Clin Invest 1988;81: Bendahan D, James Y, Salvan A, Badier M, Comfort-Gouny S, Guillot C, et al. Combined electromyography 31 P-magnetic resonance spectroscopy study of human muscle fatigue during static contraction. Muscle Nerve 1996;19: Dalakas M, Elder G, Halett M, Ravits J, Baker M, Papadopoulos N, et al. A long-term follow-up study of patients with poliomyelitis neuromuscular symptoms. N Engl J Med 1986;314: Grimby G, Einarson G, Hedberg M, Aniansson A. Muscle adaptive changes in post-polio subjects. Scand J Rehabil Med 1987;21: Agre J, Rodriguez A. Neuromuscular function: a comparison of symptomatic and asymptomatic polio subjects to control subjects. Arch Phys Med Rehabil 1990;71: Trojan D, Gendron D, Cashman N. Stimulation frequencydependant neuromuscular junction transmission defects in patients with prior poliomyelitis. J Neurol Sci 1993;118: Sharma K, Kent-Braun J, Mynhier M, Weiner M, Miller R. Excessive muscular fatigue in the postpoliomyelitis syndrome. Neurology 1994;44: Borg K, Henriksson J. Prior poliomyelitis-reduced capillary supply and metabolic enzyme content in hypertrophic slow-twitch (type I) muscle fibres. J Neurol Neurosurg Psychiatry 1991;54: Grimby G, Stålberg E, Sandberg A, Sunnerhagen K. An eight year longitudinal study of muscle strength, muscle fiber size and dynamic electromyogram in individuals with late polio. Muscle Nerve 1998;21:
7 776 ELECTROPHYSIOLOGY OF FATIGUE IN LATE POLIO, Sunnerhagen 16. Trojan D, Gendron D, Cashman N. Anticholinesterase-responsive neuromuscular junction transmission defects in postpoliomyelitis fatigue. J Neurol Sci 1993;114: Stålberg E, Trontelj J. Single fiber electromyography in healthy and deceased muscle. New York: Raven Press; Sunnerhagen KS, Hedberg M, Henning G-B, Cider Å, Svantesson U. Muscle performance in an urban population sample of men and women years of age. Scand J Rehabil Med. In Press. 19. McComas AJ, Kereshi S, Quinlan J. A method for detecting functional weakness. J Neurol Neurosurg Psychiatry 1983;46: Allen G, Gandevia S, Neering I, Hickie I, Jones R, Middleton J. Muscle performance, voluntary activation and perceived effort in normal subjects and patients with prior poliomyelitis. Brain 1994;117: Allen G, Gandevia S, Middleton J. Quantitative assessments of elbow flexor muscle performance using twitch interpolation in post-polio patients: no evidence for deterioration. Brain 1997;120: Grimby L, TollbäckA, Müller U, Larsson L. Fatigue of chronically overused motor units in prior polio patients. Muscle Nerve 1996;19: Rodriguez A, Agre J. Electrophysiologic study of the quadriceps muscle during fatiguing exercise and recovery: a comparison of symptomatic and asymptomatic postpolio patients and controls. Arch Phys Med Rehabil 1991;72: Westerblad H, Lee J, Lännergren A, Allen D. Cellular mechanisms of fatigue in skeletal muscle. Am J Physiol 1991;261:C Trojan D, Gendron D, Cashman N. Electrophysiology and electrodiagnosis of the post-polio motor unit. Orthopedics 1991;14: Sjögaard G. Potassium and fatigue: the pros and cons. Acta Physiol Scand 1996;156: Garner S, Hicks A, McComas A. M-Wave potentiation during muscle fatigue and recovery in man and rat. J Physiol (Lond) 1986;377:108P. Suppliers a. Chattanooga Group Inc., PO Box 489, Hixson, TN b. AB Detector, Box 11426, S Göteborg, Sweden. c. Red Dot 2239 monitoring electrodes; 3M Medica, Gelsen Kircher Strasse 11, D Borken, Westfalen, Germany. d. NB-MIO-16L9; National Instruments Corp., Bridge Point Parkway, Austin, TX. e. Punos Electronic AB, Knipplag 6, S Göteborg, Sweden. f. Keypoint; Medtronics, Copenhagen, Denmark.
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