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Chapter XI NEUROPATHOLOGICAL PREDICTIONS OF RECOVERY William R. Lyons and Barnes Woodhall A. INTRODUCTION Collaborative histopathological studies on peripheral nerve injuries were begun by the present authors in 1944 at Walter Reed General Hospital with a number of objectives: (1) to obtain and record the histopathology in a well-studied, representative series of human peripheral nerve injuries treated by suture; (2) to forecast regeneration on the basis of careful histopathological study of the mirror images of the sutured ends and to correlate these forecasts with eventual clinical recovery; (3) to provide the surgeon with a pathologist's advice as an aid in achieving good nerve ends preparatory to suture; and (4) to make a histopathologic study of human nerve degeneration and regeneration and to develop a photographic record of these changes. Surgical decision was implemented by gross and his- tologic reports on over 600 lesions; the first and fourth objectives were largely attained with the publication of the Atlas of Peripheral Nerve Injuries (46) to which reference may be made for a technical discussion of histologic method; the second objective defines the scope of the present chapter. Many factors are thought to influence peripheral nerve regeneration; the neuropathologist was asked to make an intensive study of one of them, the surfaces joined by the surgeon in his definitive repair, with the assurance that there would be available for correlation studies not only clinical evaluations of eventual recovery but in addition such other details of the injury and its management as might also have an influence upon end- results. Since the pathological specimens were necessarily obtained at the time of suture, and by that tokt n independently of the clinical assessments of recovery 5 years later, it was not difficult to isolate the neuropathologist from all but the very earliest follow-up data and thus to preserve the integrity of his independent predictions based on the appearance of the nerve ends. Furthermore, since correlation studies could proceed only 499

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after follow-up information had been obtained, it was natural to place in the hands of a disinterested third party, the statistician for the follow-up study, the actual task of correlation. In providing the surgeon with assist- ance at the time of repair, of course, the neuropathologist did obtain information on the nature and extent of the injury and on the details of management, together with a modicum of data on the early postoperative picture, but he made a conscientious effort to avoid being influenced by this information and to base his evaluations solely on the specimens and the slides. It was anticipated that any independent, predictive information which the neuropathological studies might contribute could easily be combined with similar information provided by other variables so as to make the best predictions possible as well as to determine the relative contributions of the various predictive variables. At the time the sampling plan for the follow-up study was crystallized, it may be recalled from chapter I, a special effort was made to allocate to the follow-up centers an appreciable number of men on whom histologic studies had been made. The entire roster (AFIP Accession No. 110,822) was used in this process, and at the conclusion of the study it was found that, of the 2,554 men used in the main statistical analysis, 356 had been allocated from the roster with histologic studies. Of the 356 men, 253, or 71 percent, were examined. In some of the latter group histologic studies were incomplete, the lesions were treated by neurolysis, partial suture, or graft, or a second suture had been necessary for which no histologic material was available. After all such cases were deleted there remained for study 181 complete sutures on the 7 major nerves, and these furnish the material for the present chapter. Table 243 contains for reference a listing of each case giving most, but by no means all, of the individual characteristics analyzed here. The 26 among them which are discussed in the Atlas (46) are cross-referenced to the latter by page. 500

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Table 273.—Summary Forecast of Regeneration and Skin Resistance, Ulnar and Peroneal Nerves Operated on Only Once Ulnar P eroneal ' Forecast (percent) Elevated skin resistance Normal, decreased skin resistance Elevated skin resistance Normal, decreased skin resistance Total Total 0-12 ... 1 o 1 3 o 3 13-22 2 o 2 2 o 2 23-32 2 0 2 1 3 4 33-42 1 0 1 0 0 0 43-52 4 3 7 6 3 9 53-62 3 2 5 2 1 3 63-72 8 5 13 3 2 5 73-82 .... 0 2 2 0 1 1 93- 0 0 0 0 0 0 Total 21 12 33 17 10 27 1 Including sciatic component. 4. Motor Recovery It will be recalled from chapter III that motor recovery may be ap- proached via several indices, the most summary being the modified British classification which is subject to some center variation. Although the most reliable motor observation is the measured strength of individual muscles, the more summary indices were explored first, and only after it became apparent that any relationship between the forecast and motor recovery was probably weak were tabulations extended to a few representative muscles as a final check. Table 274 provides a summary of the relationship between the neuropathologist's forecasts and the British classification. At best the evidence there seems suggestive in the statistical sense; only for the peroneal is the discrepancy of any real magnitude. The tabulations were then extended by introducing the eight control variables. Most of these resulted in some strengthening of the evidence of association between fore- cast and motor recovery in the upper extremity, but were without effect in the lower extremity. The evidence of association seen in table 274 for the peroneal is reflected in each of the 8 separate tables and to about the same extent, whereas none of the control variables provides more evidence of association in the tibial than table 274 shows for this nerve. The control variables which seem best able to support the association between forecast and motor recovery are site (for ulnar lesions) and number of operations (for median lesions), and table 275 presents the tabulated detail. Parallel data for peroneal lesions are given in table 276 for all lesions studied, since 559

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none of the control variables improved the evidence of association between forecast and recovery. Taken all together the evidence points to a definite but somewhat weak association between the neuropathologist's forecast and motor recovery. Motor recovery in the lower extremity was also explored on the basis of number of affected muscles able to contract voluntarily at the time of follow- up, with substantially the same results as were obtained with the British summary of motor recovery. The muscles studied in this way, and their classification as proximal or distal, are discussed on pages 106-113. Table 277 provides the mean values of the neuropathologist's forecasts for cases classified as to number of affected muscles able to contract voluntarily at follow-up. Again the evidence of association is at least suggestive for peroneal injuries, but within the range of chance variation for the tibial. Table 275.—Summary Forecast of Regeneration and British Classification1 of Motor Recovery, for Median and Ulnar Lesions With Specified Controls Median, operated upon only once Ulnar at or below elbow Forecast of regeneration A' B' A" BI 0-12 0 1 0 0 0 0 1 0 2 5 3 1 1 0 3 0 3 4 4 0 0 0 0 3 0 2 3 6 0 0 13-22 23-32 33-42 1 43-52 2 53-62 2 4 0 0 63-72 73-82 83-92 Total 10 12 15 14 Moan rating 51.6 66.2 48.5 54.5 1 In every case calculated here proximal muscles were acting against gravity, so that two classes were denned on the basis of the modified British scale: A—Proximal muscles acting against gravity or against resistance, intrinsic muscles showing at most perceptible contractions. B—Both proximal and distal muscles contracting against resistance. These correspond to the following rubrics given in detail on page 115. A—Groups 2 and 3. B—Groups 4, 5, and 6. 408980—07 18 561

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Table 276.—Summary Forecast of Regeneration and British Classification of Motor Recovery, for All Peroneal and Sciatic-Peroneal Sutures British summary of motor regeneration ' Forecast of regeneration Perceptible contraction in proximal muscles, none in intrinsics No con- traction A B Total 0-12 . . 1 2 4 1 4 0 1 0 0 2 0 2 2 7 2 0 0 0 0 1 2 0 0 0 0 0 1 1 0 0 3 3 8 3 15 4 5 1 0 13-22 23-32 33-42 0 4 1 3 1 0 43-52 53-62 . ... 63-72 73-82 83-92 Total 13 15 12 2 42 Mean rating 34.2 39.3 49.6 62.5 41.8 1 Rubrics A and B have the meanings specified in table 275. Table 277.—Mean Summary Forecast of Regeneration and Number of Affected Muscles ' Contracting Voluntarily at Follow-up, Peroneal and Tibial Injuries Peroneal and sciatic - peroneal Tibial and sciatic- tibial Number of muscles contracting Number of nerves Mean fore- cast (per- cent) Number of nerves Mean fore- cast (per- cent) A. Four proximal muscles affected 0-3 27 13 34.7 52.6 14 8 41.5 45. 1 4. . . Total 40 40.5 22 42.8 0 B. One distal muscle affected 22 10 46.9 1 38.5 Total 32 44.3 1 In standard list of muscles (p. 73). 562

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In planning the statistical correlations of pathological assessments and motor recovery it was thought unnecessary to provide for analyses based on individual muscles, and the design of the punchcards proceeded accord- ingly. However, one of the motor fields contains the average power of distal muscles in the standard set, and two nerves are represented by single muscles, the median by the abductor pollicis brevis and the tibial by the interossei. In view of this specificity it was decided to study the average power of distal muscles 2* in relation to the summary pathological rating. In the lower extremity there is too little variation in the power of movement against resistance for this approach to have any value, but for the upper extremity the results of the correlation study are as follows: No. of Correlation coefficient l Nerve lesions P \fr-Hian 24 +.27 >.05 Radial 16 + . 12 >.05 Ulnar 48 + .22 >.05 All three combined 88 + .22 .05 1 Product-moment coefficient. All three independent coefficients are small and positive, with none outside the chance range; in the aggregate they have a probability of .05 under the hypothesis of independence. There is, then, only borderline evidence of association between the summary forecast and actual power at follow-up. 5. Overall Functional Evaluation As described in the following chapter, functional performance was evaluated with the aid of an 11-point scale (0, 10, . . . 100 percent) de- veloped by Dr. Lewey, and as the most summary evaluation of recovery it seemed attractive to compare the neuropathologist's forecasts with these functional ratings. The material was tabulated separately for the upper and lower extremities and table 278 gives the mean summary forecast for each point on the scale of useful function. For neither upper nor lower extremity lesions is there statistical evidence of association. 6. Composite Index of Nerve Regeneration Except for Dr. Lewey's functional rating, the foregoing analysis deals with single modalities of recovery, and it was thought desirable to test the pathologist's summary rating against a composite index of regeneration less dependent upon the performance of useful functions. Pain, touch, SR, and motor recovery were chosen as the bases for this index, and a ** The distal muscles are specified on p. 73. 563

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simple dichotomy defined for each nerve and for each modality so that all nerves might be combined. Pain: Median and peroneal: threshold of 30 gm. or more v. <30 gm. Ulnar and tibial: threshold of 40 gm. or more v. <40 gm. Radial: threshold of 20 gm. or more v. 50 gm. v. 50 gm. or less. SR; All nerves: elevated in autonomous or total area v. normal or decreased SR. British Motor: All nerves except sciatic-tibial: no more than perceptible contraction in intrinsici v. intrinsics moving against resistance. Sciatic-tibial: no return in intrinsics v. any return in intrinsics. Table 278.—Mean Summary Forecast of Regeneration and Overall Functional Evaluation at Follow-up Upper extremity Lower extremity Scale of function Number of cases Mean forecast Number of cases Mean forecast 0 1 2 3 5 2 14 18 22 23 9 1 5 3 0 0 0 4 7 15 25 21 2 0 28 10 50 37 54 45 59 55 55 48 67 40 20 30. .. 40 34 26 50 60 46 48 42 70 80 90 58 100 Total 100 54 77 42 If each such dichotomy is represented as 0 or 1, depending on whether recovery is poorer (0) or better (1), then the lesions on each nerve or group of nerves will fall into 16 subgroups ranging from 0000 (poorer in all 4 modalities) to 1111 (better in all 4). The dichotomies were designed to facilitate the combination of the several nerves, and for purposes of analysis the 16 subgroups were combined on the basis of the number of 1 's, ranging from none to 4. From the tabulated result which appears in table 279 the only possible conclusion is that the predictive value of the summary forecast is not improved by combining the four modalities in this fashion; the vari- ation among the means presented there is well within the range of chance.

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E. SUMMARY Over 600 cases of peripheral nerve suture were studied during World War II by an histologist working with a group of neurosurgeons with a view to evaluating the microscopic quality of sutured ends. The records of the findings have been deposited in the form of reports, photomicrographs, microscopic sections, etc., in the Armed Forces Institute of Pathology. An effort has been made to forecast peripheral nerve regeneration on the basis of this material, and these predictions have been correlated with the results of follow-up examinations made in the five clinical centers as part of the larger follow-up study. The mechanics of correlation have been in the hands of the statistician for the follow-up study. Table 279.—Mean Summary Forecast of Regeneration and Composite Index of Regeneration Number of modalities with regeneration rated favorably Number of lesions Mean rating 0 18 48.33 1 33 51.67 2 37 49.59 3 31 52.90 4 6 53.33 Total 125 50.96 Follow-up status was represented by the pain and touch thresholds, skin resistance, several indices of motor recovery, and overall functional recovery. Not all functions subserved by the periphal nerves were represented, and those that were represented often were only partially covered, as in the restriction of observations on pain and touch to the autonomous zones. Nevertheless, if the follow-up observations be regarded as a sam- pling on the basis of which recovery might be roughly scaled, the represen- tion of modalities would appear to be adequate for the present purpose. The neuropathologic assessments were made in terms of changes in four regions of the nerve, seen in cross section: epineural, interfascicular, peri- neural, and intrafascicular. The neuropathologist evaluated the fibrous or neuromatous changes evident in each individual region and assigned to that region a numerical value representing the relative loss in recovery he ex- pected from these defects. He did not make separate forecasts for fine fibers carrying pain and autonomic impulses and for the larger fibers carrying pressure, touch, and motor impulses. For each segment (distal or proximal) the estimates for all four regions were summed to represent the anticipated influence of all the defects present in that segment. The overall rating was then obtained on the assumption that the defects in the two segments were independent; specifically, the complements of the estimated

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percentage losses for the two ends were multiplied to provide a numerical estimate of recovery for the nerve as a whole. It was, of course, regenera- tion across the gap at which the predictions were aimed; other character- istics of the lesion and associated injuries were known and could be inte- grated with the neuropathologic assessments as required. Any such index is undoubtedly an arbitrary one, and it may seem presumptuous to apply a percentage scale to the pathologic phenomenon of fibrosis in different cross- sectional areas of nerves. However, the most that was hoped for was that in its clinical application the overall summary might permit a rough segre- gation of cases into those with good, bad, and indifferent nerve ends. Analysis of the neuropathologist's ratings on the 181 nerve lesions studied here shows that the intrafascicular region of the distal segment is the chief source of variation in the final estimates. The severest penalties were always applied to the nerves with more advanced degrees of distal tubular shrinkage, and it was rare that defects in other regions were considered prejudicial to any appreciable extent. The ratings vary somewhat by nerve, chiefly in that those of the upper extremity were given a better chance of recovery than those of the lower. The ratings were not found to vary by site of lesion, but both the length of gap and time interval from injury to suture were seen to be inversely correlated with the neuropathologist's overall estimates of regeneration. The correlations have been sought for each modality or other index of recovery, separately by nerve and for all nerves combined, but without developing more than suggestive evidence of association. Various charac- teristics of the lesion and its handling, e. g., time and length of gap, have also been introduced as control variables, but without adding appreciably to the evidence of association. Summary tables are included as a record of these analyses, together with a master table showing the necessary data for each lesion. On balance the view is taken that a definite association probably does exist, especially for SR and voluntary motor function, but that the relationship is too weak for clinical usefulness. As already noted, the severest penalties were always applied to the nerves showing the most advanced degrees of distal tubular shrinkage, a phenome- non shown to be pronounced 5 months or longer after nerve severance. There were 30 cases with poor assessment ratings, and in the correlation tables they were equally distributed among good, bad, and indifferent classes of muscle recovery. Since voluntary motor fibers are usually con- sidered to be large in caliber and well myelinated, the good and fair results under adverse histologic circumstances suggest that shrunken neurilemmal tubules may be redistended, or that voluntary contraction of muscle may be accomplished even though the effector fibers may not regain their normal girth or state of myelination. Case reports, including illustrations, have been presented for a represent- ative group of cases. The photomicrographs of the nerve ends have provided what may be regarded as the most plausible explanation of the poor functional results in cases considered to have had little or no pathologic

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alterations in the nerve ends at the time of suture. The mismatching of proximal and distal fascicles, an invariable result of the resection and suture of nerve stumps, has been demonstrated, and is considered to be a most important factor in producing imperfect redistribution of nerve fibers and, therefore, subnormal functional recovery. On the rare chance that the above findings be wrongly interpreted as evidence against careful resection to good tubules preparatory to anasto- mosis, it must be pointed out that the range of variation in the quality of nerve ends studied here is actually a small one. Had surgeons not uni- formly cut back the injured segments to achieve the best ends they could provide within the limitations imposed by the gaps to be bridged, the results reported here, and in the motor chapter where a small effect seemed associated with the quality of the nerve ends, would probably have been very different. On an absolute scale, nerve ends range in quality from those produced by the surgeon's scalpel to the blunt, neuromatous bulbs commonly presented to the surgeon exploring war injuries. Only the better part of this absolute range is adequately represented in the material studied here, and the findings, therefore, pertain only to that part of the range. They must not be taken as any discouragement to painstaking resection preparatory to anastomosis. 567

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