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Chapter IV ELECTRICAL EVIDENCE OF REGENERATION Harry Grundfest, Y. T. Oester, and Gilbert W. Beebe A. INTRODUCTION Numerous electrodiagnostic tests have proved useful in the study of pe- ripheral nerves, both experimentally and clinically. Their clinical value is especially great preoperatively in evaluating the chance of spontaneous recovery, at operation when the surgeon is confronted with the necessity for deciding whether to lyse and leave alone or resect and suture, and later when there may be doubt concerning the progress of regeneration following suture. Inclusion of electrodiagnostic tests in the standard list of follow-up observations was prompted by no strong expectation that they would prove as useful in the evaluation of late results as they are in making early assess- ments, but rather by the belief that the opportunity should not be missed for comparing their results with those obtained in the study of voluntary movement. Also, there was some hope that electrical studies might throw additional light upon cases classified as failures in motor recovery on the basis of examination of voluntary movement. In retrospect it would also appear that the addition of the electrodiagnostic battery to the standard workup most probably served to improve the quality of the motor studies. Discrepancies between voluntary movement and electrical responses prompted more careful study of individual muscles, and at times alerted examiners to disparities between anatomical reinnervation and functional recovery which could be turned to patients' advantage. Since the follow-up studies were made about 5 years after injury, neither early nor interim observations could be procured under the design adopted for the study. However, in chapter XII, where electrodiagnostic tests are reviewed from the standpoint of their contribution to surgical diagnosis, early and longitudinal observations are given on the basis of a subsequent study of casualties from the Korean episode, made by Nulsen at Valley Forge General Hospital. In accordance with the original plan for the analysis of the follow-up data, a complete, separate study was made of the electrical observations along the lines already described in chapter III for voluntary motor recovery. 203

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The standard muscles specified for routine electrodiagnostic tests are those listed in table 48, plus the following: Paroiual and sciatie-peroneal Extensor digitorum brevis Peroneus brevis Tibial and sciatic-tibial Flexor digitorum brevis The content of the present chapter is of more limited scope, however, and for these reasons: (1) The selection of muscles for certain of the electro- diagnostic tests depends so much upon the results of voluntary stimulation that no fair comparison of any two sets of cases could be made without prior assurance of the comparability of their selection, and in practice this means that the analysis of responses to these tests must rest upon the studies of voluntary movement; (2) to the extent that electrical and voluntary data correlate, a separate presentation of motor recovery seems superfluous; (3) the electrical data are so much less extensive than those on voluntary movement that explorations based on the latter are considerably more powerful; and (4) the electrical data are much more subject to center variation than the observations on voluntary movement. Furthermore, the chief clinical value of the electrodiagnostic tests at the point in time at which the follow-up study was done lies in the contribution they make to an understanding of the factors associated with absence of voluntary movement. Accordingly, the electrodiagnostic data are studied here, not as independent evidence on the presence or absence of nerve regeneration, but as auxiliary information of especial value in illuminating some of the factors which may be responsible for the absence of voluntary movement. B. METHODOLOGY Essentially four electrodiagnostic tests comprise the standard battery: 1. Stimulation of the nerve. 2. Chronaxiemetry. 3. Galvanic tetanus ratio. 4. Electromyography. In the coding of data for the statistical analysis provision had also been made for recording the EMG response to stimulation of the nerve, but this observation was made on only one percent of the individual muscles in- volved in the study and merits no further consideration. Finally, although not an electrodiagnostic test in the same sense as the four listed above, direct muscle stimulation was performed as a means of assessing muscular atrophy 1. Stimulation of Nerve Monopolar or bipolar electrodes are applied to the skin overlying a motor nerve or are inserted subcutaneously to lie close to or enter the sheaths of the nerve. Electrical stimuli of controllable, graded intensity are applied through the electrodes, either as brief, single shocks or as a train of repetitive 204

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excitation. In the different follow-up centers they were variously derived from the capacity-type chronaxiemeter, single or multiple shock square pulse generators, or from an alternating current source (including faradic stimulation). The type of stimulus employed is relatively unimportant provided the strength can be controlled so that an adequate and safe stimulus is delivered to the nerve. The test ascertains whether the nerve is in functional continuity with a muscle capable of contraction. The sources of discontinuity may be: a. Absence of anatomical regeneration in the nerve; b. Absence of reinnervation of the muscle; or c. Absence of muscle fibers. The first two conditions could be detected by observing presence or absence of nerve impulses, but this was not done in the present study. Chronaxi- emetry, which was extensively carried out, provides the same information in a technically more convenient manner. In the course of the latter test also direct stimulation of the muscle provides information regarding the presence or absence of muscle as well as the nature of the response of the muscle fibers. Stimulation of the nerve rapidly delimits the functionally intact from the nonfunctional neuromuscular groups. Together with observations on voluntary movement it also provides a clear-cut differentiation between those neuromuscular groups which are not used by the patient because of anatomical defects and those which are not used because of psychic or learning factors. The latter categories of nonuse should not be minimized. In the course of this study it has been found that even experienced observers sometimes attribute to failure of anatomic regeneration a lack of movement apparently caused only by some psychic factor or by a failure in relearning the use of a muscle or even a digit. Of particular value in early diagnosis is the stimulation of the nerve at two levels, one above and one below the site of injury. In some instances following gunshot injury, when the nerve is in gross continuity, local propa- gation-block may cause a temporary paralysis which simulates anatomical loss of continuity. This condition may, however, be temporary, lasting up to 3 to 4 months. When temporary, it does not result in neural degenera- tion and the muscles involved remain excitable to neural stimulation applied below, but not above, the site of block. When block without degeneration is present some 2 weeks after injury it would appear to be preferable to delay surgical intervention until some opportunity for recovery has been provided, since recovery, if it occurs, then takes place without major disruption in the organization of the neuromuscular or the sensory complex, whereas after neurosurgery this occurs inevitably to some extent (5, 44, 61, 66). In all, observations were made on 6,264 individual muscles, about 40 percent of all those involved in the present study. There were, in addition, 185 individual muscles in which the observation could not be made because an adequate stimulus could not be tolerated. The extent to which direct 205

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Table 114.—Percentage of Affected Muscles Examined by Nerve Stimulation, Complete Sutures on All Seven Major Nerves, for Muscles With Studies of Voluntary Movement, by Center Center None Voluntary movement Any Total Total Nerve stimu- lation done ' Total Nerve stimu- lation done ' Total Nerve stimu- lation done ' Num- ber Per- cent Num- ber Per- cent Num- ber Per- cent Boston 224 259 583 728 116 92 1 539 403 9 41.1 0.4 92.5 55.4 5.4 629 747 1,733 1,897 897 204 3 32.4 853 1,006 2,316 2*625 1,063 296 4 2,220 1,086 34.7 0.4 95.9 41.4 3.2 New York . ... 1,681 683 25 0.4 97.0 36.0 2.8 34 Total . . 1,960 1,044 53.3 5*903 2,596 44.0 7,863 3,640 46.3 1 Exclusive of those few in which nerve stimulation was attempted but the current could not be tolerated. nerve stimulation was performed in each center, and the presence of bias in the selection of cases for such stimulation, are shown in table 114, which is confined to 7,863 muscles supplied by the 7 major nerves, complete nerve sutures, standard muscles affected by injury, cases with movement not affected by tendon transplant, by loss of muscle substance by direct injury, or by sacrifice of a nerve branch, and muscles in which an examination of voluntary movement was made. Only in the New York center was direct nerve stimulation routine and the selection of muscles for testing quite unbiased, and in only three centers was nerve stimulation done on any appreciable number of cases. In the aggregate 46 percent of the muscles included in table 114 were examined by direct nerve stimulation, but somewhat more often (53 percent) in cases with no voluntary movement than in cases with voluntary movement (44 percent). The muscular activity induced by stimulation of the nerve was scaled as follows, for each muscle: No contraction. Contraction Barely visible. Similar to voluntary contraction. Stronger than voluntary contraction. Of the entire set of 6,264 muscles observed following stimulation of the nerve, contractions were observed in 71.4 percent. By type of contraction 206

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this total breaks down as follows: 12.9 percent barely visible, 53.4 similar to voluntary contraction, and 5.1 stronger than voluntary contraction. All statistical analysis has been based on the percentages with at least visible contraction and with no contraction. 2. Chronaxiemetry Principles The theoretical basis of chronaxiemetry can be simply stated, although many of the details remain unclear. With the exception of certain synapti- cally activated systems, every excitable tissue (e. g., nerve, muscle, sense organ) can respond to an electrical stimulus of adequate strength. Stimu- lus thresholds, however, are a function of duration (figure 17). A liminal stimulus of very brief duration will be of higher intensity than one of long duration. However, all excitable tissues possess the property that a stimu- lus of relatively long ("infinite") duration cannot be effective when reduced Figure 17. Change in chronaxie with the size of the stimulating electrode1 I 200 100 § 1000 1 - 200 100 CAPILLARY CATHODE O-021/.F-O-OS.'i AGCI-WIRE CATHODE NERVE JjJJSCLE NERVE MUSCLE I I I I I 0.001 0.002 0.005 0.01 0.02 0.05 0.1 0.2 0.5 O.I 'The single nerve-muscle fiber preparation of the frog retrolingual membrane; monopolar stimulation of either the nerve or the muscle fiber. The abscissa plots the logarithm of the various capacities used in the stimulating circuit. 1.0 jjF is equivalent to 4.0 msec. (or in the older form a). The ordinates plot (in relative units) the logarithm of the minimal voltage to which a given capacitor was charged to excite the tissue. When the punctate stimulating cathode was a fine saline-filled capillary* the upper Itrength duration curves were obtained yielding chronaxies of 0.04 msec. for stimulation of the nerve fiber* and 0.12 msec. for one of the muscle fibers innervated by that nerve fiber. The lower curves were obtained when the same pair of units were stimulated with a large chlorided silver wire placed close to the nerve or muscle fiber. The chron- axie of the latter, 2.1 msec. now had increased almost 20-fold, while the chronaxie of the nerve fiber (0.08 msec.), had only doubled. (From Grundfest (28), reprinted by permission from the Journal of Physiology.) 207

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below an intensity which is specific for the type and condition of the tissue and for the nature of the stimulation. The minimal threshold for a stimulus of infinite duration defines the "rheobase" (38). It provides an easily de- termined quantity, the intensity of the stimulus when the duration of the latter need not be accurately determined, provided it is sufficiently long. Given the rheobase, which furnishes an intensity unit of the stimulus, a single point on the curve of the strength-duration relationship can then be determined which serves as a useful characterization of that curve. That point is the "chronaxie," and it may be defined as the minimal duration of a stimulus with an intensity twice the rheobase. The chronaxie is charac- teristic of the excitable tissue. Numerous studies have been published (6) on the chronaxie for different neuromuscular groups in normal and diseased conditions. In man the chronaxie of such normal units usually falls in the range below 1 msec. (millisecond) and most frequently below 0.5 msec. When neuromuscular transmission is eliminated as in nerve degeneration (also in neuromuscular block by curare, etc.) the chronaxies obtained may be in the range of scores of msec. The explanation of this difference has generated considerable dispute. Lapicque (38) believed that the anatomi- cal or pharmacological changes produced an alteration in the strength- duration relation which was reflected in the increase of the chronaxie. Others (28, 65) demonstrated, however, that the normal strength-duration curve of innervated muscle fibers is much more dependent on the conditions of stimulation than is that of the nerve fibers, a major factor being the area of the tissue which is being effectively stimulated. In motor nerve fibers this effective area of stimulation is limited by their myelinated, noded struc- ture, whereas the muscle fiber can be electrically stimulated everywhere on its surface. Therefore, under the conditions of percutaneous stimulation, where the effective electrode is a large surface, the chronaxie of direct elec- trical stimulation of the muscle is large, while that of the nerve is small. Normally, percutaneous stimulation applied to a motor point excites prima- rily nerve fibers, yielding a low chronaxie. When the muscle is denervated, however, only direct stimulation of its fibers is possible, and under the con- ditions of stimulation the chronaxie obtained is high. As reinnervation proceeds, the chronaxie decreases from the large values of the denervated muscle through various intermediate values, and tends to return toward the normal, low value when reinnervation of the whole muscle has taken place. No entirely satisfactory explanation of this phe- nomenon is available. At least one factor resides in the nature of the ob- servations. The measurements are carried out by suitable stimulation of a motor point, with the observer striving for a minimal contraction of the muscle under study. In visual observation the response is probably com- posed of neurally evoked activity of a number of motor units as well as of directly stimulated nonreinnervated muscle fibers. It is, therefore, likely that the magnitude of the chronaxie will depend on the relative proportions of th e differently excited elements and will decrease progressively as that proportion shifts more and more in the direction of completely neural acti- 201

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vation. However, this may not be the complete explanation. Denervated fibers may have themselves undergone prolongation of chronaxie as their excitable properties were altered. If the return to normal excitability were gradual after reinnervation the observed chronaxie would likewise decrease gradually. Usefulness Whatever the theoretical explanations of the effects might be, it is evident from this study as well as from earlier work that chronaxie is closely corre- lated with regeneration of the neuromuscular complex. The progressive decline of the chronaxie in the course of successive examinations, therefore, gives an early indication of progress in reinnervation, and is accordingly a useful index. Indeed, it is also possible sometimes to detect the approximate degree of reinnervation of a given muscle. For example, the regrowth of only a small bundle in a motor nerve may be detected by the appearance of a localized region of the muscle possessing a lowered chronaxie while the rest of the muscle, which remains denervated, exhibits a high chronaxie. In the hands of an experienced observer the differences in these values, and also in the appearance of rapid twitches of the reinnervated muscle fibers and slower contraction of still denervated muscle fibers, furnish valuable information. At a single examination, such as characterized this study, chronaxiemetry has a more restricted usefulness, since it can then only reflect the current state of reinnervation or its absence. However, it provides in this connection some critically useful information: a. The character and degree of the response of directly excited muscle fibers provide a rough estimate of the state and amount of activable muscle tissues. b. The magnitude of the chronaxie gives an estimate of the degree of reinnervation. It is a more quantitative test of the intactness of the neuromuscular organization than is neural stimulation, but is more time-consuming and requires a more highly trained operator. c. The finding of a low chronaxie in the face of functional paralysis may indicate the nature of this loss of function. As with nerve stimulation, but in a more quanti- tative manner, it may indicate presence of a propagation block in the nerve, of psychogenic paralysis* of loss of the learned processes of muscle movement (by virtue of disruption of these patterns by long absence of use* or by virtue of anatomical alterations in the pathways), or of malingering. Methodology The chronaxiemeters used in this study fall into two classes, which do not differ basically in the data they can furnish. The electrical pulses generated may be rectangular as produced by a variety of electronic means. The amplitude may be controlled to provide a source of variable voltage or, as in the Golseth-Fizzell instrument (26) used by the Boston and Chicago centers, the stimulator provides a source of controllable current which is maintained at the desired level of output despite variation in the resistance offered by the electrode or by the tissues of the patient. In theory it may be preferable to use the latter "constant current" type of stimulation, but under actual conditions the advantage is doubtful. In 209

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clinical measurements the stimulus is applied percutaneously, and the pathway for the current includes a variety of tissues, in addition to the nerve and muscle. Each of these tissues is polarizable and probably to a different extent. The instantaneous stimulating current through the excitable tissue will therefore be complexly determined by the polarization of the different components. At any rate, it would appear that measure- ments with "constant current" and "constant voltage" pulse generators are essentially equivalent. Short rectangular pulses (i. e., those below 0.5 msec. in duration) are easily distorted by the electrical properties of the stimulating electrodes and by the tissues of the patients. Furthermore, reproducibility of dura- tions to the second decimal place (i. e., 0.01 msec. in the lowest range of durations) is poor with most electronic circuits. Some centers, therefore, have used stimulators which deliver discharges of condensers charged to a controlled voltage. The theory of the capacitative chronaxiemeter is discussed fully by Lapicque (38). His measurements and many others have demonstrated that the magnitude of the capacity is directly converti- ble into durations for any given stimulating circuit. The capacitor chronaxiemeters used in this study were capable of delivering pulses varying accurately by increments of 0.01 msec. The techniques of chronaxiemetry are described in various textbooks (6, 38) and will not be dealt with here. It is, however, necessary to stress that the apparently simple procedure hides a number of pitfalls. Obser- vation by some of us of the measurements made during and after World War II by technicians in military hospitals indicates that much more than routine training is required. The measurements depend to some extent on the accurate placing of electrodes, on correct treatment of these, on the rate at which observations are repeated, and on the experience of the operator in observing and evaluating the response. Even in the hands of the usually experienced examiners of the different follow-up centers results varied too greatly to permit the data of all five centers to be pooled directly. Table 115 illustrates this variation on the basis of data on the abductor digiti quinti following complete suture of the ulnar nerve. There were in all 5,581 chronaxie determinations on individual muscles, or about 36 percent of all the muscles involved in the study. If attention is confined to the 7 major nerves, complete sutures, standard muscles affected by injury, muscles with movement not influenced by sacrifice of a nerve branch, by direct loss of substance through injury, or by tendon transplant, and muscles in which studies of voluntary movement were made, it appears that 44 percent were tested by chronaxiemetry. However, as may be seen in table 116, the centers varied widely in their resort to chronaxiemetry, and in every instance their selection of muscles was a biased one. In the aggregate 25 percent of the muscles incapable of voluntary movement were tested by this means in comparison with 51 percent of the muscles capable of voluntary contraction. 210

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Table 115.—Center Variation in Chronaxie Determinations on Abductor Digiti Quinti Following Ulnar Nerve Suture New York and San Francisco Boston and Chicago Philadel- phia Chronaxie, in msec. Percent 60.5 Percent 1.0 Percent 17.9 00 01-02 27.2 54.7 39.3 03-07 11.1 22.1 31.0 08-12 1.2 13.7 9.7 0 8.4 2. 1 Total . . . 100 0 99 9 100 0 Number of muscles 162 95 145 Table 116.—Percentage of Affected Muscles Studied by Chronaxiemetry, Complete Sutures on All Seven Major Nerves, Muscles Studied for Voluntary Movement, by Center Voluntary movement Center None Any Total Total Chronaxie- metry done Total Chronaxie- metry done Total Chronaxie- metry done Num- ber Per- cent Num- ber Per- cent Num- ber Per- cent Boston 224 259 583 728 166 25 47 228 166 26 11.2 629 747 1,733 218 170 1,349 733 520 34.7 22.8 77.8 38.6 58.0 853 243 217 1*577 899 546 28.5 21.6 68.1 34.2 51.4 Chicago 18.1 39.1 22.8 15.7 1,006 2*316 2,625 1,063 New York Philadelphia 1*897 897 Total 1,960 492 25.1 5,903 2*990 50.7 7,863 3,482 44.3 3. Galvanic Tetanus Ratio The tetanus ratio (TR) is based upon two quantities which may be ob- tained in the course of stimulating muscles directly by means of galvanic current: (a) the current required to produce a sustained contraction, or tetanus; and (b) the rheobase or current required to produce a minimal contraction. In human skeletal muscles with normal innervation the tetanus ratio is usually about 3.5 to 4.0, and the normal range is generally

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taken as 3.0 to 5.0. During a period of complete denervation the ratio approaches and may actually reach unity. During a period of reinnerva- tion the ratio rises sharply, generally markedly above normal values, and as reinnervation progresses it slowly falls to within the normal range. Determinations are made by applying conventional electrodes to the skin overlying the muscle to be tested. A constant-current generator, with an output in the range of milliamperes, and capable of maintaining a fixed output in the face of changes in the resistance of local tissues, is used to stim- ulate a minimal twitch. The current is then increased until the muscle responds with a sustained contraction (tetanus) during the entire time the current is applied, usually 4 seconds. The current required to produce tetanus is then divided by the current required to produce the least muscle twitch, and the resulting ratio is the tetanus ratio. Although the tetanus ratio was included in the standard battery of tests agreed to by all investigators, determinations were not often made and for a variety of reasons. In all, determinations were made on 1,138 muscles, regardless of type of injury, extent of surgery, or sampling area. On muscles affected by complete suture, for lesions in the representative sample, 11 muscles were tested often enough to permit some exploration of bias asso- ciated with the selection of muscles for testing. Contraction on voluntary stimulation was employed in this investigation, which showed that the TR was more often sought in the presence of voluntary contraction than in the presence of none, so that the set of muscles with TR values is not itself an unbiased set. For example, 18.3 percent of upper extremity muscles ob- served to contract voluntarily have TR readings in contrast to 12.6 percent of those with no voluntary contraction; this discrepancy has a probability of .03 in the statistical test employed here. For the lower extremity the dis- crepancy is smaller and by itself well within the range of chance, but both discrepancies, considered jointly, have a probability of about .025. Where- as in the particular representative sample of upper extremity muscles used here 11 percent failed to contract voluntarily, in the set with TR readings the figure is 7.7 percent. The bias is not, therefore, large enough to be very troublesome. Of greater interest is the relation between voluntary contraction and TR. Although the present series is not large enough to exhibit this relationship hi any detail by nerve, it does include an adequate number of readings on the abductor digiti V and, moreover, as may be seen from figure 18, the same average relationship appears to characterize this muscle and all others taken together. An adjustment has been made for the selection of muscles for TR determinations, so that the curves of figure 18 are free from this defect. In the region of TR readings below 3.0 the percentage with volun- tary contraction rises rapidly from about 50 to 90 percent, and continues to rise thereafter but more slowly. In the region of TR about 6.0 or more voluntary contraction is very nearly complete. Although the TR readings were studied in relation to a number of char- acteristics of injury and treatment, for the reasons already mentioned the 212

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213

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Table 124.—Voluntary Movement, Response to Direct Nerve Stimulation, and Chronaxie Determinations, for All Affected Muscles Following Complete Sutures on all Seven Major Nerves, Philadelphia Center1 None Voluntary movement Any Total Chronaxie, msec. Contraction follow- ing nerve stimula- tion Contraction follow- ing nerve stimula- tion Contraction follow- ing nerve stimula- tion None (1) Any (2) Total (3) None (4) Any (5) Total (6) None (7) Any (8) Total (9) Total 307 248 59 3 2 3 1 7 96 41 55 3 5 5 5 6 1 8 403 289 114 70 54 16 2 1 4 613 286 327 55 58 48 15 34 11 18 4 43 1 40 683 377 302 75 5 3 7 1 9 2 5 709 327 382 58 63 53 20 40 12 26 4 52 1 53 1,086 629 Unknown . . . 340 343 57 59 52 15 36 13 18 4 43 1 45 457 63 66 60 21 49 14 31 4 65 1 83 0 6 7 8 6 13 1 13 1 2 3 . . . . 4 2 2 5 6 5 7 8 13 9 22 13 9 >10 25 13 38 5 30 1 Only muscles with observations on both voluntary movement and response to direct nerve stimulation are included. When a division of the chronaxie scale was sought on the basis of mini- mizing disagreement with the results of direct nerve stimulation, the best division was found to be 0 to 10 v. 11 or more msec., but even on the basis of this division 27 percent of the muscles presented discrepancies between the two tests in comparison with only 6 percent in the New York center. In figure 21 the two centers are compared as to the relation between the several tests. In table 126 are shown the results of dividing the chronaxie scale in the optimum fashion just described. It will be noted that all 3 tests agree in 178 instances with minimal evidence of regeneration, and in 1,552 instances with maximal evidence. The corresponding percentages are 7 and 60, which may be compared with 16 and 72 in the New York data. If the cases in the remaining 6 cells of the table, about which the tests disagree to some extent, are allocated in the fashion described for the New York data the final estimate of the percentage with regeneration is found to be 77, slightly below the value of 81 calculated for the New York 230

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data, but well above the values of 72 percent obtained from the data on voluntary contraction alone and 71 percent obtained from the observations on direct nerve stimulation. The numerical discrepancy between the estimates of the two centers is not too important because there are also differences between them in the emphasis they placed upon the examina- tion of specific muscles, and these differences are not taken into account here. The chief lesson of the analysis is the same for both centers, namely that the best estimate which can be made from the data on all three tests is about what may be obtained from the joint observations on voluntary Table 125.—Voluntary Movement, Response to Direct Nerve Stimulation, and Estimated Distribution of Chronaxie Values, for All Affected Muscles Following Complete Sutures on All Seven Major Nerves, Philadelphia Datal None Voluntary movement Any Total Chronaxie, msec. Contraction follow- ing nerve stimula- tion Contraction follow- ing nerve stimula- tion Contraction follow- ing nerve srimula- tion None (1) Any (2) Total (3) None (4) Any (5) Total (6) None (7) Any (8) Total (9) Total 555 28 19 28 9 66 173 9 16 16 16 19 3 25 728 193 24 1,686 284 299 247 77 175 57 93 21 222 5 72 1,879 308 311 296 77 199 81 93 21 222 5 84 748 52 31 77 9 90 24 47 1,859 293 315 263 93 194 60 118 21 250 5 75 2,607 345 346 340 102 284 84 165 21 373 5 144 9 173 0 37 35 44 25 85 3 72 1 12 49 2 3 4 24 24 5 6 47 7 8 123 28 151 123 9 10 57 9 3 60 9 12 69 9 11 12 75 9 84 12 77 89 87 86 13 14 12 10 22 12 10 22 15 16 47 19 66 12 21 33 59 40 99 17 >18 47 10 57 12 26 38 59 36 95 1 In view of selection of muscles for direct nerve stimulation as well as chronaxie, the estimates were developed to reflect the entire sample of muscles with tests for volun- tary movement, not merely those tested both for voluntary movement and induction of movement by direct nerve stimulation. 231

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8 8 9 8 8 R 8 ft f ft I I 232

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contraction and response to direct nerve stimulation on the following assumptions: a. Muscles which move voluntarily are innervated (i. <-.* errors of positive findings in neurological examination are absent); b. Muscles which do not move voluntarily but do contract on direct nerve stimu- lation are innervated (i. e., positive results of the electrical test are valid); and c. Only those muscles which contract in neither are denervated. In the New York center about 21 percent of the muscles examined by means of voluntary and direct nerve stimulation were also studied by means of electromyography, and in the Philadelphia center about 19 percent. In both centers there was a marked tendency to avoid electromyographic study of muscles unable to contract voluntarily or on direct nerve stimu- lation, as may be seen in table 127, which pertains to muscles affected by complete suture and on which both voluntary and direct nerve stimulation was performed. Although the eleciromyographic observations are quite sparse, it was thought that they might be useful in distinguishing between muscles which Table 126.—Estimated Distribution of Affected Muscles by Voluntary Contraction, Response to Nerve Stimulation and Chronaxie Group, Philadelphia Data Chronaxie group, msec. Response to direct nerve stimulation None Any Total A. No voluntary contraction (MO 377 11 or more 178 Total 555 B. Voluntary contraction 0-10 145 11 or more 48 Total 193 C. All muscles 0-10 522 11 or more 226 Total 748 135 38 173 512 216 728 1*552 134 1,686 1,697 182 1*879 1*687 172 1,859 2*209 398 2*607 403930—BT- -17 233

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could not be moved voluntarily because of failure in regeneration and those in which absence of voluntary movement might be attributed to other factors. Electromyographic studies on the 33 muscles shown in table 127 as incapable of voluntary movement at the New York center usually showed no more than fibrillation potentials if direct nerve stimu- lation produced no contraction, and motor unit potentials if direct nerve stimulation resulted in contraction. Table 128 provides the details of this relationship. The very high correlation exhibited there lends considerable support to the validity of the interpretation that failure of voluntary move- ment is not a direct measure of failure of peripheral nerve regeneration. Table 127.—Choice of Muscles for Electromyographic Study in Relation to Voluntary Movement and Results of Direct Nerve Stimulation, by Center Results of stimulation New York Philadelphia Muscles with electromyo- graphic studies Muscles with electromyo- graphic studies Voluntary Direct nerve Total muscles Total muscles Number Percent Number Percent None None 120 98 19 1,319 17 16 2 291 14.2 16.3 10.5 22.1 51 51 15 288 4 3 2 68 7.8 5.9 13.3 23.6 None Contraction.. . . None Contraction Contraction Contraction.. . . Total 1,556 326 21.0 405 77 19. 0 Table 128.—Electromyographic Interpretations and Response to Direct Nerve Stimulation for Muscles With No Voluntary Movement, New York Data Electromyographic interpretation Response to direct nerve stimulation None Contraction Total At most fibrillation 13 1 14 Motor unit potentials 4 15 19 Total 17 16 33 The analysis of electromyographic data from the New York center was carried one step farther by introducing chronaxie as a fourth variable. It is unfortunate that the data are so few (table 129). They do suffice to 234

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show a very intimate association between chronaxie and electromyographic interpretation: % cases with at most fibrillation had chronaxies of 6 or more, and tf%it cases with motor unit potentials had chronaxies below 6. In the main, also, table 129 reveals all 3 electrical tests to be in moderately good agreement and to point to the necessity for regarding muscles in- capable of voluntary contraction as a mixed group, some denervated and some not. The electromyographic data are too few to provide any in- dependent basis for making that distinction, but do at least roughly con- firm the distinction based on the results of nerve stimulation and chron- axiemetry. The only discrepancy of note consists of the 4 muscles with motor unit potentials but no movement either voluntarily or on nerve stimulation and chronaxies of 6 or more. One of these 4 was interpreted as "few motor unit potentials with voluntary effort" and 3 as "spontaneous fibrillation potentials plus some motor unit potentials, and no complex or other potentials." Since potentials of the latter variety were noted in only about 8 percent of the 284 with motor potentials and movement on both voluntary and direct nerve stimulation, these 3 cases are not typical of those with motor unit potentials and they will hardly serve to challenge the testimony of the other 2 electrical tests. Table 129.—Electromyographic Interpretations in Relation to Voluntary Stimu- lation, Direct Nerve Stimulation, and Chronaxie, New York Data Contraction Chronaxie 0 to 5 msec. Chronaxie 6 or more msec. Voluntary Direct nerve stimu- lation At most fibrilla- tion Motor unit po- tentials At most fibrilla- tion Motor unit po- tentials None None 1 0 0 2 0 8 2 284 12 1 0 0 4 7 0 5 None Some Some None Total Some 3 294 13 16 2. Estimated Influence of Factors Preventing Voluntary Contrac- tion The method outlined in the preceding section provides a tool for esti- mating likelihood of reinnervation and for estimating the frequency with which psychological and neurological processes outside the neuromuscular complex may have impeded the voluntary contraction of reinnervated muscles. Table 130 contains these estimates for muscles of chief interest following complete suture, and is confined to cases in the representative 235

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jy« -3 Ji g-g 1 oo in NO 00 CM r- 3 RI 3 > a-lT! s I •* co ON o m ON Isg n *• U 1 §?! JS ill 151 1 u-X 1 § 1 T3 | O C ^ CM CM CM -as 9 °^3 * -H c3 5i: |f 1 1 CM r- m * r^ NO Sjf- H -* m CM CM GO O ^* CM CM a isi PI g oo eo m CM •* r- ^- eo CM -*• • * -o •* a li t M* o ;j ON o o * r*- CM 1 •2 O GO ON 00 ON 00 00 J4 M U C > g* o II d C? O If O S— ' O oo r* - co co c s -j ^ ' § 2 >-3 6 •^ o •7 •-H ^1 N_^ i i * s E h £ o* co m oo •-i NO rv) co NO oo *-i CM to CM g, ** S t; - 0 NO co IF i NO NO ON T3 «T3 i i co CM ^I " "* n § U J9 2 X a * •JP i T Q ^* •- — co -52 I i fc -^ 1 I 3 -3 |||| ^ S S88 in *-i ON 1 O C* GO h 1 1 E liil NO 00 CM y 1 S PJ CO *Q ON ON •» •!•? C C || E 1 i^gi ^ cN r*J oo t- oo •^j- in co s U IT) 00 OO 00 § §| i l§i 1 y NO c'l CT1 in ^ co 73 g 1 2 es CO iri oo oo co — — 1 1 JB 'o I i H •J .^— . r oo — ON 00 t*- i 1 £ " 00 OO 00 1 I IS r~ r- oo c s •o m in r* NO >§ 1 3 ON 00 CN] | •^ w •-» 1 1*1 3 ESS •" ^ O « — Comparative Esi I 1 I.S * : 2 *. : fc I?i E < 43 d Median .... T- ^ i i J J3 23«

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to Cv! CM co oo in eg ve co ^ eN vo oo r- ~ •* •* O •* oJ 00 CO O 00 » * # ^ r- m co .- 0) ^i C M "SS in NO c^ ^— • -—• N.X *H •* N m CM oo m 5^ '^ c** O T• r^ N C M 00 O ON Tj - CO cs cq rg *-• m ^- t- T-i T-I ON NO W Scs oN T« in co vo ^- C M cs C M r- •* cs o r- •* o OO NO 00 ?•* CM ON TT -• NO 00 •« ov ON r- eg CM in r- O •1 N 00 vO ^- l*- r* C M r- o oN §e^ •* 1*- t*- ^H r^ oo CM o ~ oo oo r- oo *-• *-- *-• ^ CO cO CO S25 *-• T-• T^ •-i -" T-- CM- * Ov CO CN 00 GO m vo •*• *-• r^ ^o vn i*- •* vo r- ON co in m m T|- co m Tf OO OO Ov CN O) 00 NO CO ON NO •O oo m r^ oo r~ ON r- *-i •* oo oN oN r^ oN CO 00 ON CO CO CO ON CO Ov •* cv r- oo cs co co »H ON O r- in f ov r-- m ON ON ON ON •-i•-iTH r^ ON r- •»? CNT ON t^ ON 00 t- f- - ON 00 NO 00 in oo oo co in in oo o r- o vo t*- vo r- i*- •* •<- 00 CM O C M n n co t^ C^ CO co r- *-i CM" --T co" * * 0O •* ov •-i oo £^ I^C* •f o « c- »5-v^ ON NO r- — co *-J •*' V vo vc JLIxt/ oN oo r^ o CO •,«, •* •* oo T-. C M '-. CM *-t *- CM •- N oj m co • T-. CM co * m cs CM •* in t-- o r- *-• ^^ ^- CO 1^ 0 U-. — T •* vO 0) O £££ cs vo in * oo m o CM *-i ^- C - 33 r- ^ in r- t^ m co vo ON CO * O *-^ NO ON NO r^ O C?. --0 m *H •-i -Tr •* •» c o T OO 00 O C- - O Ov 00 CM I*- ON oo ON r- Tr r^ CM r-- •* CM r- in in vo in C M in in >-i *-i •-i ON oo eo oo oo r- O »H l*- C M £££ o in o oN t^ m co in CM co in in •* co t*- NO CO NO ON CO CO CO' NO O oo in r^ NO r- ON NO m •* CO 00 d ON •*• CO O CO 00 00 O m ov m co NO * CM m ON NO P- CM CM • * ON •* CO •* *-i ^i NO •* T-« CO OO CM O co co m 00 O ON .-i •* r- ON NO CM ON C^ OO 00 r- vo •* vO » » » in •* CN in ON CM CM oo in NO v_x v- ' ^_x S- r~ in ro ov vo *-> oo r • oo S22: >- ON O T- 0 CM NO in m •* CO •M •* in co CM •* r- * TI •» m r* - 00 S 3 S « oo fs co ^- T* CO ON -^ O ON 00 00 ON $33 ON •* CO CM 00 *-« 00 r~ NO ill • bi g> : -Si* *!•§ "> c : §1 g> i ** * ji ill fe.*| iJ-^g1 s.a>^'° JJJ j S .tf^-9. 8 .Sf^ u -a ex « T3 J3 c C T3 J3 355 P^tSi O E E Pill 3 •• - < < O W « W O b t* Radial Tibial |-a 2 •a •43 II i |3 vS 1,1 •h-2 „ a }< u i i I C u S +«* i

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sample. It also contains, for comparative purposes, the following additional estimates: a. The percentage reinnervated, using as the basis of estimate the percentage contracting voluntarily for all muscles in the representative sample, not merely those in which direct nerve stimulation was done; b. The percentage reinnervated, using as the basis of estimate the percentage con- tracting on direct nerve stimulation; and c. The percentage of cases in which voluntary contraction was blocked by psycho- logical and learning factors* estimated from data on all complete sutures, not merely those in the representative sample. The estimates based on either voluntary contraction alone or response to nerve stimulation alone do not differ appreciably in the aggregate, but occasionally large discrepancies are noted for individual muscles. When the estimates of columns 3 and 5 of table 130 were correlated, the correlation coefficient was found to be + .96,w and the equation for the best-fitting straight line is: Y=-7.90+1.1 IX where Y denotes the percentage contracting voluntarily and X the per- centage contracting on direct nerve stimulation. Figure 22 contains a plot of these percentages. The estimates in column 7, reflecting the as- sumptions stated above and the methodology developed in the preceding section, are considered to be the best estimates for the muscles tabulated, except possibly for the fact that there is some slight bias in the selection of muscles for testing by direct nerve stimulation. However, the bias is considered too small to warrant any further adjustment of the estimates of column 7. On the average, 23 percent of the muscles unable to contract volun- tarily were observed to move on direct nerve stimulation; for the repre- sentative sample of sutures the figure is 22 percent. Individual muscles are not represented by enough cases to permit an extensive comparison of muscles, and to compare nerves on the basis of all muscles combined raises problems of the independence of one muscle from another on the same limb. Accordingly, comparisons have been made to only a limited extent and on the basis of individual muscles in a fashion suited to the assumption of independence of all observations combined together. The specific comparisons made, and their results, are as follows: a. The various nerves, with each represented by the muscle with the largest number of cases in which voluntary movement was not possible* provided there be at least 25 such cases, i. e., Median—abductor pollicis brevis Ulnar—1 st dorsal interosseus Peroneal—extensor hallucis longus Sciatic-peroneal—extensor hallucis longus Sciatic-tibial—flexor hallucis longus These muscles are clearly not homogeneous as to the proportion, among all incapable of voluntary movement, which contract on direct nerve stimulation: the median and ulnar muscles more often contract on electrical srimulation. 15 It should be noted that this coefficient has been obtained on a set of percentages* i. e., averages, which mask a certain amount of individual variation. The corresponding coefficient applicable to individual muscles, as estimated from the four-fold table of voluntary contraction by response to nerve stimulation, is +.89. 238

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Figure 22. Percentage of Affected Muscles Contracting Voluntarily After Com- plete Suture, and Percentage Contracting on Direct Nerve Stimulation PERCENT PERCENTA8E CONTRACTING VOLUNTARILY PERCENT WO 90 80 70 60 50 30 20 10 T I (EACH POINT REPRESENTS A MUSCLE) I I -LINE OF IDENTITY I I I I I I 10 20 30 40 50 60 70 80 PERCENTA6E CONTRACTING ON NERVE STIMULATION 90 100 90 80 70 60 30 20 10 100 b. The abductor pollicis brevis and the 1st dorsal interosseus are obviously quite similar. c. Peroneal and sciatic-peroneal lesions were compared on the basis of each muscle. For the extensor hallucis longus the peroneal lesions have an advantage, but for the other three peroneal muscles the percentage is higher for sciatic-peroneal. However, for only one muscle (extensor digitorum longus) is the discrepancy a statistically significant one (P about .03), and for the material as a whole it would seem best to take the position that the sciatic-peroneal and the peroneal do not differ. d. The two sciatic components were compared on the basis of the extensor hallucis longus and the flexor hallucis longus and appeared not to differ by more than chance expectation. The muscles chosen to represent the upper extremity (abductor pollicis brevis and 1st dorsal interosseus) are, of course, distal muscles while those chosen to represent the lower extremity in the first comparison (a) are proximal muscles, and there may be some confounding on that account. Distal muscles in the lower extremity were not tabulated in this fashion, 239

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and proximal muscles in the upper extremity are represented by too few cases to settle the matter; we know only that the five sets of cases studied in the first comparison (a) differ quite significantly. The foregoing comparison provides a test of the hypothesis that the proportion of muscles able to contract on direct nerve stimulation, among muscles unable to contract voluntarily, is constant from nerve to nerve, muscle to muscle. Perhaps an even more meaningful hypothesis to test is that the proportion of muscles unable to contract voluntarily, among all those innervated, is constant from muscle to muscle and nerve to nerve. The latter proportion is given in columns 9 and 16 of table 130, from which comparisons may be made rather directly. Column 9 is limited to the representative sample of complete sutures, while column 16 applies to all complete sutures for which both voluntary and electrical stimulation was attempted. The evidence of the two columns is the same, and since column 16 rests on many more cases it may be used as the basis for any comparisons. It seems clear, without formal test, that the proportion of reinnervated muscles which do not contract on voluntary stimulation is much higher in the lower extremity than in the upper, and especially for muscles affected by sciatic lesions. However, among the muscles of the lower extremity the gastrocnemius and soleus (following injury to the sciatic-tibia!) has an exceptionally low percentage in relation to other muscles of the lower extremity. In summary, then, table 130 provides the best estimates available in this material of the likelihood of reinnervation and, given reinnervation, of the chance that contraction will not occur on voluntary stimulation. The latter varies by nerve and to some extent by muscle within the set innervated by a given nerve, in that it is much higher in the lower ex- tremity than in the upper, and that among muscles of the lower ex- tremity, the gastrocnemius and soleus are atypical. 240