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Muscle Recovery in Poliomyelitis

W. J. W. Sharrard, London, England

From the Institute of Orthopedics and the Royal National Orthopaedic Hospital.

The Journal of Bone and Joint Surgery, Vol 37 B, No. 1, February 1955:63-79.

Lincolnshire Post-Polio Library copy by kind permission of Professor Sharrard.

How much recovery will take place? For how long will improvement continue? In every case of paralytic poliomyelitis these two questions are asked. Some would echo Courtney (1896) in answering that "the disease is so variable that it is very difficult to say anything about prognosis at all." While this may be the correct answer during the acute stage of the disease, it should be possible, after the first four weeks, to give a less guarded reply.

With the development of manual methods of muscle testing first introduced by Lovett and described by his assistant Wright in 1912, the grade of paralysis of a muscle may be defined in terms that allow the progress of its recovery to be followed. In recent years results obtained by these methods have been analysed to show the extent of muscle recovery in poliomyelitis (Harry 1938, Carroll 1942, Lenhard 1943, Watkins 1949, Green 1949, Grossiord and Husson 1953). Though these studies indicate the general potentialities for recovery in paralysed muscles, their usefulness in clinical practice is limited. In most, the muscles investigated have been too few and the tests too infrequent to allow the progress of muscle recovery to be followed in detail. The recovery of individual muscles has received attention from only one author (Skinhøj 1949) and differences that may exist in the rate of recovery at different ages have not been investigated.

The object of this paper is to show how a knowledge of muscle recovery may be of practical value in the management of patients in the convalescent stage of poliomyelitis.

MATERIAL AND METHOD

Between November 1949 and December 1950, 185 patients who had suffered a recent attack of paralytic acute anterior poliomyelitis were admitted to the Stanmore section of the Royal National Orthopaedic Hospital. In 149 patients the onset of the paralysis had occurred less than thirty-two days before admission. These were the cases in which a three-year study of recovery was begun.

Each patient was examined on ten occasions, at one, two, four, six, eight, ten, twelve, eighteen, twenty-four and thirty-six months after the onset of the paralysis. A complete muscle test was made on each occasion. So far as possible, testing was always performed with the patient in a warm room, after rest. Standard methods of manual muscle testing were used (Daniels, Williams and Worthingham 1947; Kendall and Kendall 1949). The grade recorded depended upon the power of a muscle in the third of three contractions through the greatest range of movement of the joint concerned. The scale of muscle power ranging from 0 to 5 recommended by the Medical Research Council (1942) was used during the making of the observations, though, for reasons given below, it was modified in the analysis of results. All the tests were made by the author.

At the end of three years a complete follow-up had been obtained in 142 patients, seven of the original number having moved to a distance too great to justify repeated attendances for examination.

All the patients received the same treatment during the investigation. This was the standard treatment given at the hospital and consisted in daily passive movements to the joints and active exercises to the muscles of an affected limb up to, but not beyond, the point of fatigue. After three to four months, increasing functional activity was added to the regime in most cases, with diminishing attention to individual muscles. The duration of in-patient treatment varied between one month in cases of mild paralysis of one upper limb, and two years or more in severely paralysed individuals. The mean duration of active physiotherapy was ten months.

The accuracy of manual muscle testing --The investigation of muscle recovery by manual methods has recently been the subject of some criticism by those who advocate a return to mechanical methods of measurement of muscle power (Russell 1952) -- notably that, in the assessment of the power of a muscle, it is not certain that two observers will assign the same grade to it.

In.most muscles and muscle groups the Medical Research Council scale can be used to give an unequivocal result. An incorrect assessment is almost always due to ignorance of the method, inattention to detail, lack of appreciation of the action of the muscle under test, or the deception of the trick action of another muscle. A high degree of objectivity is necessary in manual muscle testing; all too frequently the task is delegated to the physiotherapist who is treating the patient, and the desire to record an increase in power may supersede the strict evidence of the test.

Ideally, therefore, muscle tests should be made by someone who does not see and treat the patient every day. They should be performed without reference to the results of previous tests and the same observer should be responsible for all the tests in a given patient. It is true that the assessment of the power of certain muscles, such as the muscles that act upon the digits, is difficult to make in the exact terms of the Medical Research Council scale and is partly dependent on the pure judgement of the particular observer; even so, the assessments of that observer should be consistent.

Table I
The Distribution of Paralysis in Muscles of the Lower Limb

Muscle Total of all grades of paralysis
one month after the
onset of the paralysis
Number completely paralysed
three years after the
onset of the paralyis
Hip flexors 198 34
Hip abductors (gluteus medius and minimus) 201 47
Hip adductors 193 36
Gluteus maximus 203 33
Biceps femoris 202 54
Inner hamstring muscles 204 43
Quadriceps 204 46
Tensor fasciae latae 189 38
Tibialis anterior 182 103
Tibialis posterior 169 89
Peronei 165 60
Extensor hallucis longus 157 66
Extensor digitorum longus 161 63
Triceps surae 162 57
Flexor hallucis longus 154 84
Flexor digitorum longus 155 85
Intrinsic muscles of the foot 140 24

In this investigation I have checked the constancy of my own muscle testing by occasionally repeating a test after an interval too short for any recovery to have taken place, so that the results of the second test should have been identical with those of the first. The muscles listed in Tables I and II, and included in the analysis to follow, gave constant results. The results for some muscles, such as the small rotator muscles of the hip, serratus anterior, and the muscles of the trunk, proved to be unreliable and were therefore excluded from the analysis. On rare occasions the results of muscle tests could be compared with the findings in muscle at necropsy. The proportion of residual normal muscle fibres always corresponded well with the clinical assessment in the muscles listed in Tables I and II. In muscles that were unreliable in the clinical test the clinical grade was often at variance with the necropsy findings.

An enormous mass of data resulted from the observations, there being over 110,000 individual assessments. At the first examination there were 3,033 muscles in 211 lower limbs and 1,905 muscles in 126 upper limbs whose power had been graded as less than normal. It is the progress of recovery in these muscles that will now be described.

Table II
The Distribution of Paralyis in Muscles of the Upper Limb

Muscle Total of all grades of paralysis
one month after the
onset of the paralysis
Number completely paralysed
three years after the
onset of the paralyis
Trapezius 81 3
Pectoralis major 108 9
Deltoid 127 25
Lateral rotators of shoulder 107 14
Latissimus dorsi 95 11
Triceps brachii 118 15
Elbow flexors 97 10
Extensor carpi radialis longus 69 17
Extensor carpi radialis brevis 67 8
Extensor carpi ulnaris 65 7
Extensor digitorum 66 8
Extensor pollicis brevis 65 10
Abductor pollicis longus 65 12
Extensor pollicis longus 68 5
Pronators 68 11
Flexor carpi ulnaris 62 12
Flexor carpi radialis 68 16
Flexor pollicis longus 58 8
Flexor digitorum profundus 56 2
Flexor digitorum sublimis 56 5
Opponens pollicis 75 30
Flexor pollicis brevis 66 23
Abductor pollicis brevis 75 30
Interossei 63 13
Hypothenar muscles 60 16

The uniformity of the Medical Research Council scale of muscle power -- Because the power of a muscle is denoted by a numeral it is tempting to imagine that the figures bear a mathematical relationship to one another. Although, from the arbitrary nature of the system of grading, any such relationship would be coincidental, the clinical impression gained from experience in muscle testing is that some uniformity does exist in the " steps " between one grade and the next: that, for instance, the amount of recovery indicated when a muscle increases in power from grade 2 to grade 3 is comparable with that when it increases from grade 3 to grade 4. The data from this study have been used to deduce mathematically whether this is the case.

The proportions of muscles in grade 1 that reached grade 2, of grade 2 muscles that reached grade 3, of grade 3 muscles that reached grade 4, and of grade 4 muscles that reached grade 5 in the interval between the first and second muscle test (one to two month interval) were calculated. Proportions were worked out in the same way for the two to four month, four to six month, and six to eight month intervals. During any of these intervals, the proportion of grade 4 muscles that increased in grade was consistently about one-half that of any of the other grades; that is to say, while it was as easy for a muscle to proceed from grade 1 to grade 2 as from grade 2 to grade 3 or as from grade 3 to grade 4, it was nearly twice as great a step for it to proceed from grade 4 to grade 5.

A second analysis was then made in which muscles that had been assigned a grade of 4+ were considered as being in a separate grade; the possible moves in grade that could occur were then: 1 to 2, 2 to 3, 3 to 4, 4 to 4+, 4+ to 5. The results using this modified scale showed that a surprising uniformity now existed in the steps between all the grades.

As a result of this finding, all muscles previously designated grade 4+ were rechristened grade 5, and all those of grade 5 became grade 6. The new 0 to 6 scale, in the terms of which subsequent analyses were made, becomes:

0 = No contraction.
1 = Flicker or trace of contraction.
2 = Active movement with gravity eliminated.
3 = Active movement against gravity.
4 = Active movement against gravity and some resistance.
5 = Active movement against gravity and considerable resistance.
6 = Normal power (within the limits of manual assessment).

THE RATE OF RECOVERY IN THE MUSCLES OF THE LOWER LIMB

Of the 3,033 lower limb muscles of all grades of paralysis at the first muscle test 962 remained completely paralysed (grade 0) throughout the three-year period. These irrecoverable muscles never partook in the process of recovery and were, therefore, separated from the total. Evidence from muscle biopsy and necropsy suggests that permanently paralysed muscles are completely denervated at the acute stage of the disease, and findings in the anterior horn of the spinal cord support this view (Sharrard 1953). The remaining 2,071 muscles form a "working total" in which recovery during the one to two month interval may be calculated.

The unit of recovery in this analysis is an upward move in grade. An upward move of one grade, as from grade 2 to grade 3, represents one unit of recovery; an upward move of two grades as from grade 2 to grade 4, represents two units of recovery. The total number of such moves in grade between the one month and two month muscle test was found to be 1,128; that is, 54·5 per cent of the working total of 2,071 recoverable muscles.

At the two month muscle test sixty-one muscles had reached grade 6 and, so far as muscle testing was concerned, had become incapable of further recovery. This number was subtracted from the original total of 2,071 muscles to give a new working total of 2,010 muscles for the calculation of recovery in the two to four month interval. The total number of upward moves in grade during this period was 1,114, that is 55·4 per cent of the working tota of 2,010 muscles. But this proportion of muscles recovered during a period of two months, so that the rate of recovery per month becomes 27·7 per cent.

Fig 1 Histogram
Fig. 1
The rate of recovery in the muscles of the lower limb.

The rate of recovery at subsequent intervals was calculated in the same way; the results are shown in histogram form in.Figure 1. From a high initial figure the rate of recovery falls rapidly at first and then more gradually until, at the twelfth month, less than 5 per cent of muscles move in grade each month. At this time, fourteen-fifteenths of the total possible recovery has taken place.

No increase in grade was observed after the twenty-fourth month except in rare instances. Thus after the correction of a position of deformity at a joint a muscle that was previously working at a mechanical disadvantage or had been subject to overstretching was able to increase its activity and power. It must be emphasised, though, that twenty-four months does not necessarily mark the end of functional recovery, to which no final date can be given in any one patient.

Fig 2 Histogram
Fig. 2
The rate of recovery in the gluteus maximus.
[203 Muscles; 33 Permanently Paralysed]

Fig 3 Histogram Fig 4 Histogram
Fig. 3 Fig. 4
The rate of recovery in the biceps femoris.
[202 Muscles; 54 Permanently Paralysed]
The rate of recovery in the tibialis anterior.
[182 Muscles; 103 Permanently Paralysed]

The same method of calculation was used to discover the rate of recovery in the seventeen individual muscles of the lower limb. Figures 2, 3 and 4 show the results found for gluteus maximus, biceps femoris and tibialis anterior. The interesting and unexpected finding is that all the individual muscles of the lower limb show almost identical rates of recovery, both in the shape of their curve and in their absolute data. The impression gained from clinical observation had been that the rate of recovery differed in individual muscles. For instance, the peronei appeared to recover better than the tibiales, and the gluteus maximus better than the quadriceps.

The reason for this impression can be seen from inspection of Table I: those muscles that show poor clinical recovery include a high proportion of permanently paralysed muscles among their number, whereas those that show apparently better recovery include fewer permanently paralysed muscles.

THE RATE OF RECOVERY IN THE MUSCLES OF THE UPPER LIMB

The same calculations were made to determine the rate of recovery in the 1,905 upper limb muscles. The results, shown in histogram form in Figure 5, are very like those for the lower limb, though the rate of recovery is about 5 per cent per month higher in the upper limb at any time interval up to the tenth month.

Fig 5 Histogram
Fig. 5
The rate of recovery in the muscles of the upper limb.

Fig 6 Histogram Fig 7 Histogram
Fig. 6 Fig. 7
The rate of recovery in the flexor carpi ulnaris.
[62 Muscles; 12 Permanently Paralysed]
The rate of recovery in the flexor pollicis longus.
[58 Muscles; 8 Permanently Paralysed]

Fig 8 Histogram Fig 9 Histogram
Fig. 8 Fig. 9
The rate of recovery in the deltoid muscle.
[127 Muscles; 25 Permanently Paralysed]
The rate of recovery in the elbow flexors.
[97 Muscles; 10 Permanently Paralysed]

The individual muscles of the upper limb show parallel rates of recovery, though with slightly more variation between each other than was present in the lower limb muscles. The results in the forearm and hand muscles, represented by flexor carpi ulnaris (Fig. 6) and flexor pollicis longus (Fig. 7) follow the pattern of the upper limb muscles as a whole (Fig. 5); but in the shoulder musculature, particularly in the deltoid muscle (Fig. 8), the rate of recovery falls suddenly at the fourth month and then increases slightly up to the tenth month, after which it falls to less than 7 per cent per month. The upper arm muscles, represented by the elbow flexors (Fig. 9) show curves of recovery intermediate between the two patterns.

Abduction splints were applied in many cases when paralysis in the upper limb affected the abductors of the shoulder. It is possible that the retarded recovery in the deltoid muscle between the fourth and eighth months was due to the wearing of these splints (Knowleden and Sharrard 1955). The enhanced recovery between the eighth and tenth months coincides with the time at which many of the splints were discarded.

As in the lower limb, the apparently poor power of recovery in such muscles as the thenar group of muscles and the deltoid muscle depends on the larger proportion of permanently paralysed muscles among their number (Table II).

RECOVERY IN RELATION TO AGE

The curve of recovery shown in Figure 1 is an average curve for all patients of all ages. Some patients appeared to recover more rapidly than others, completing the bulk of their recovery by the tenth month. Others recovered more slowly than the average, but continued to make significant gains in power up to or beyond the twelfth month. These variants were independent of the extent or distribution of the paralysis, but they did appear to be related, at any rate in part, to age.

Table III
Distribution of 142 Patients in Age Groups

Age group Number of patients
0 - 2 years 27
2 - 4 years 30
4 - 10 years 27
10 - 20 years 23
Over 20 years 35

A division of patients was made into five age groups, each containing a comparable number of patients (Table III). The rate of recovery was calculated in each group.

The four to ten years group and, to a less extent, the two to four years group show curves of rapid recovery (Figs. 11 and 12) whereas the over twenty years group (Fig. 14) shows slow recovery and the ten to twenty years group has an average recovery (Fig. 13).

The curve of recovery in the under two years group (Fig. 10) is especially interesting because infants of this age cannot co-operate in formal muscle re-education. Yet the pattern of recovery does not differ significantly from that in any other group and the total amount of recovery is as great as, if not greater than, that in the others. The resilience and adaptability of the infant and the fact that muscle education is one of his natural tasks probably account for this.

Fig 10 Histogram
Fig. 10
The rate of recovery in the under two years age group.

Fig 11 Histogram Fig 12 Histogram
Fig. 11 Fig. 12
The rate of recovery in the two to four years age group. The rate of recovery in the four to ten years age group.

Fig 13 Histogram Fig 14 Histogram
Fig. 13 Fig. 14
The rate of recovery in the ten to twenty years age group. The rate of recovery in the over twenty years age group.

THE PROGNOSIS FOR RECOVERY IN PARTLY PARALYSED MUSCLES

Lower limb -- In the calculation of the rate of recovery it has not been necessary to consider the actual grade of a muscle because the unit of recovery has been an increase in grade.

To estimate the amount of recovery in the muscles of the lower limb, all muscles that were assessed at grade 1 at the first (one month) muscle test were reviewed to determine their grade at the end of the investigation. Muscles assessed at grade 2, 3, 4 and 5 at one month were treated in the same way. The results (Fig. 15) show that, although a small proportion of muscles of each grade failed to improve at all, and a few gained by as much as four grades, most muscles improved by one, two or three grades. After making allowance for the fact that muscles that begin at grade 5 cannot increase in power by more than one grade, an average increase of about two grades was made by all muscles from their level of paralysis at the one month muscle test, whether their grade at that time was 1, 2, 3 or 4 (Table IV).

Table IV
Amount of Recovery Made by Lower Limb Muscles
from One Month after the Onset of the Paralysis

Grade at
one month
Mean grade at
twenty-four months
Mean increase
in grade
0* 2.2 2.2
1 3.0 2.0
2 4.2 2.2
3 5.2 2.2
4 5.9 1.9
5 6.0 1.0
* Excluding permanently paralysed muscles.

A fresh calculation was then made to discover the improvement in power of the lower limb muscles from the grade at which they had been assessed at the second (two month) muscle test. Again, a small proportion failed to improve or made a spectacular increase in power, but most improved by one or two grades (Fig. 16). An average increase of about one and a half grades was made by muscles of all levels of paralysis except those that commenced at grade 6 (Table V).

Table V
Amount of Recovery Made by Lower Limb Muscles
from Two Months after the Onset of the Paralysis

Grade at
two months
Mean grade at
twenty-four months
Mean increase
in grade
0* 1.8 1.8
1 2.5 1.5
2 3.5 1.5
3 4.7 1.7
4 5.6 1.6
5 6.0 1.0
* Excluding permanently paralysed muscles.

After the fourth month about half of the muscles of any given grade improved by one grade, a quarter of them failed to improve, and a quarter improved by two grades (Fig. 17). The average increase was one grade (Table VI). After the sixth month almost half of the muscles improved by one grade but a larger proportion, over a third, failed to improve and a correspondingly smaller proportion improved by two grades (Fig. 18). The average increase was three-quarters of a grade (Table VII).

Table VI
Amount of Recovery Made by Lower Limb Muscles
from Four Months after the Onset of the Paralysis

Grade at
four months
Mean grade at
twenty-four months
Mean increase
in grade
0* 1.5 1.5
1 2.0 1.0
2 3.0 1.0
3 4.0 1.0
4 5.2 1.2
5 5.8 0.8
* Excluding permanently paralysed muscles.

Table VII
Amount of Recovery Made by Lower Limb Muscles
from Six Months after the Onset of the Paralysis

Grade at
six months
Mean grade at
twenty-four months
Mean increase
in grade
0* 1.3 1.3
1 1.8 0.8
2 2.7 0.7
3 3.7 0.7
4 4.9 0.9
5 5.6 0.6
* Excluding permanently paralysed muscles.

The uniformity of recovery is such that it is possible to predict the further recovery that may be expected in a muscle from a knowledge of its grade at any time after one month from the onset of the paralysis. On the average the final grade of a muscle in the lower limb may be estimated by adding 2 to its grade at one month, 1.5 to its grade at two months, 1 to its grade at four months, and 0.75 to its grade at six months.

In clinical practice these figures have proved to be useful guides to prognosis. But it must be appreciated that they are mean values and that the amount of recovery can vary within the limits shown in Figures 15 to 18.

Fig 15 Histogram Fig 16 Histogram
Fig. 15 Fig. 16
Lower limb. The final grade of muscles assesed at one month from the onset. Lower limb. The final grade of muscles assesed at two months from the onset.

Fig 17 Histogram Fig 18 Histogram
Fig. 17 Fig. 18
Lower limb. The final grade of muscles assesed at four months from the onset. Lower limb. The final grade of muscles assesed at six months from the onset.

Upper limb -- The results of the same analysis for muscles of the upper limb are given in Figures 19 to 22 and Tables VIII to XI. As in the lower limb muscles, there is more variation in the final grade reached by muscles from the tests at one month and two months than from those at four months and six months.

But the amounts of recovery are somewhat greater than the corresponding ones for the lower limb muscles. On the average, the final grade of a muscle in the upper limb may be estimated by adding 2.5 to its grade at one month, 2 to its grade at two months, 1.5 to its grade at four months and 1 to its grade at six months.

Whether these figures represent a real superiority in the recovery of muscles in the upper limb over those in the lower limb, or whether they arise from differences in the technique of manual muscle testing in the limbs, is a question that this investigation cannot answer.

Table VIII
Amount of Recovery Made by Upper Limb Muscles
from One Month after the Onset of the Paralysis

Grade at
one month
Mean grade at
twenty-four months
Mean increase
in grade
0* 2.97 2.97
1 3.2 2.2
2 4.4 2.4
3 5.37 2.37
4 5.92 1.92
5 6.0 1.0
* Excluding permanently paralysed muscles.

Table IX
Amount of Recovery Made by Upper Limb Muscles
from Two Months after the Onset of the Paralysis

Grade at
two months
Mean grade at
twenty-four months
Mean increase
in grade
0* 2.5 2.5
1 3.0 2.0
2 3.9 1.9
3 5.0 2.0
4 5.8 1.8
5 6.0 1.0
* Excluding permanently paralysed muscles.

Table X
Amount of Recovery Made by Upper Limb Muscles
from Four Months after the Onset of the Paralysis

Grade at
four months
Mean grade at
twenty-four months
Mean increase
in grade
0* 2.0 2.0
1 2.2 1.2
2 3.2 1.2
3 4.4 1.4
4 5.4 1.4
5 5.9 0.9
* Excluding permanently paralysed muscles.

Table XI
Amount of Recovery Made by Upper Limb Muscles
from Six Months after the Onset of the Paralysis

Grade at
six months
Mean grade at
twenty-four months
Mean increase
in grade
0* 1.7 1.7
1 2.3 1.3
2 2.9 0.9
3 4.0 1.0
4 5.1 1.1
5 5.8 0.8
* Excluding permanently paralysed muscles.

Fig 19 Histogram Fig 20 Histogram
Fig. 19 Fig. 20
Upper limb. The final grade of muscles assesed at one month from the onset. Upper limb. The final grade of muscles assesed at two months from the onset.

Fig 21 Histogram Fig 22 Histogram
Fig. 21 Fig. 22
Upper limb. The final grade of muscles assesed at four months from the onset. Upper limb. The final grade of muscles assesed at six months from the onset.

THE PROGNOSIS FOR RECOVERY IN COMPLETELY PARALYSED MUSCLES

The further recovery of a muscle in which clinical activity can be detected during the first six months after the onset of the paralysis is almost certain. The presence of active muscle fibres implies the existence of intact motor nerve cells in the anterior horn of the spinal cord. A muscle that is clinically completely paralysed may or may not possess a few intact motor nerve cells. If it does, then, given time and favourable circumstances for muscle action and re-education, it will recover. If all the motor nerve cells that supply it have been destroyed it cannot recover.

Figures 23 and 24 show how the passage of time makes the prognosis of completely paralysed muscles more certain. One month after the onset a completely paralysed muscle had rather less than an even chance of showing some recovery; but after six months over 90 per cent of the muscles that were still clinically inactive remained completely paralysed, and, of those that did recover, less than half achieved more than a flicker of contraction. If, at any point of time, a completely paralysed muscle did show: any return·of activity, its prognosis then followed that described for partly paralysed muscles.

Fig 23 Histogram Fig 24 Histogram
Fig. 23 Fig. 24
Lower limb. The final grade of muscles completely paralysed at one, two, four and six months from the onset. Upper limb. The final grade of muscles completely paralysed at one, two, four and six months from the onset.

Though in many patients it may be appropriate to observe the progress of a completely paralysed muscle for six months to determine its prognosis, it may be important, particularly in a fairly severely paralysed limb, to have some early indication of.the likelihood of recovery·so that decisions may be made about the management of the paralysis.

Electrical tests, of which Brooks's (1953) percutaneous method of demonstrating nerve conductivity is probably the most accurate, may show the presence of intact axons supplying muscles that are clinically inactive, but they require appropriate apparatus and expert knowledge, and are not applicable to all muscles.

The destruction of motor cells in the spinal cord has been shown to occur regionally and focally (Elliott 1942, Sharrard 1953). A consequence of this is that the complete loss of all the motor cells supplying a muscle may sometimes be inferred from the presence of complete paralysis in muscles supplied by the same and adjoining spinal cord segments. Thus, the presence of complete paralysis of the quadriceps (L.2, 3, 4) and tibialis posterior (L.4, 5) indicates that a tibialis anterior (L.4) which is also completely paralysed is very unlikely to recover.

A special example of this principle applies to the completely paralysed limb in which the poor prognosis for recovery in any one of its muscles has already been recognised (Seddon 1949). In such cases the anterior horns of the spinal cord are often completely devoid of motor cells. In this series there were twenty-two lower limbs in which no muscle was active one month after the onset (except, in a few cases, for a feeble contraction in the small muscles of the foot). All the muscles in all of these limbs remained completely paralysed at the end of three years. In contrast, in the whole series 33 per cent of muscles that were completely paralysed at one month showed some recovery.

DETERIORATION IN MUSCLE POWER

A loss of power between one muscle test and the next was very uncommon. It was never seen in this series in any of the muscles of the upper limb except in the thenar muscles on three occasions, in each of which power was regained at the subsequent muscle test.

In the lower limb thirty-four instances of deterioration were observed, an incidence of 0.03 per cent. In thirty-one of these the deterioration did not continue; the muscle power either remained stationary at the next muscle test or the original power was regained. The muscles predominantly affected were extensor digitorum longus (five times), extensor hallucis longus (four times), the hip abductors (four times) and tibialis anterior (three times).

Three permanent deteriorations, in which a muscle continued to decrease in power until it became clinically completely paralysed, although initially it had been assessed at grade 2 or grade 3, were observed in tibialis anterior, extensor hallucis longus and extensor digitorum longus. In each of these instances a strong opposing force (muscle pull or gravity) was present.

DISCUSSION

The key to the understanding of muscle recovery in poliomyelitis is the division of the paralysis into a "recoverable" and an "irrecoverable" fraction whose proportions are determined in each case by the site and extent of the motor nerve cell destruction that has occurred during the acute stage of the disease.

It is the irrecoverable fraction that accounts for the variability of the disease upon which Courtney and other writers have commented. This is the factor that governs the general severity of the paralysis in an epidemic, in a patient, or in a limb, and that is responsible for the apparent differences in the power of recovery of different muscles.

When the irrecoverable fraction -- that is, the muscles that have suffered complete and permanent paralysis by loss of all the motor nerve cells supplying them -- is separated from the remainder the true picture of muscle recovery can be seen. In spite of the relatively coarse and arbitrary method of clinical measurement of muscle power used in this study, the constancy shown in the rates of recovery in muscles of diverse function and size, in patients of all ages, is as remarkable as it is significant.

Whatever the mechanisms of muscle recovery are, whether neural, muscular, or a combination of the two, they must act in the same way and to the same degree in all muscles and in all patients, however mild or severe the paralyses. In this respect the recovery of muscle in poliomyelitis differs from the recovery in peripheral nerve injuries in which factors such as the quality of the suture line and the distance of the muscle from it determine the outcome. The similarity of the curves of recovery for different muscles and the absence of any sudden spurts of recovery in poliomyelitis suggest that downgrowth of axons from the spinal cord plays no part in recovery.

The fundamental division into recoverable and irrecoverable paralysis defines the correct clinical approach to the treatment and prognosis of poliomyelitis. A patient seen one or two months after the acute disease with a scattered paralysis in which most of the muscles are in grade 2 or grade 3 can confidently be expected to make a fairly complete recovery; indeed if any muscles substantially fail to make the predicted amount of recovery, or show deterioration in power, an inhibiting factor such as an over-strong antagonist or a position of deformity should be suspected.

On the other hand if, after six months of treatment, a limb or a group of muscles in a limb still show complete paralysis, it is unfair to the patient and to the physiotherapist who is treating him to hold out false hopes of recovery. Although a remarkable measure of functional restitution may be achieved by some patients, there is no such thing as a "miracle cure" so far as individual muscles are concerned in a well treated patient.

The results of this investigation may also be applied to aid in planning the treatment of the paralysis in a given limb. For instance, in an adult, a caliper may need to be provided to give stability to the knee (in a child it may be required, in addition, to prevent deformity). In an adult lower limb in which the quadriceps shows a grade of 2 four months after the onset of the paralysis, it would be reasonable to postpone the prescription of a caliper in the expectation of recovery in that muscle to a level (grade 3) sufficient to give stability to the knee joint. In another limb in which the quadriceps is completely paralysed four months after the onset, and muscles supplied by the same spinal segments (the hip adductors and tibialis anterior) are also completely paralysed, treatment should be planned in the expectation that the quadriceps will almost certainly be permanently paralysed.

It is widely believed that if there is an inequality of muscle action at a joint, as for instance when the triceps surae is paralysed to grade 1 and the dorsiflexors of the ankle are acting at grade 3, the process of recovery may restore the balance, the weaker muscles being able to "catch up" with the stronger ones. Unfortunately this never occurs, for both muscle groups recover at the same rate and to the same degree, maintaining the disparity between each other. Even if attempts are made to restore the balance by concentrating treatment on the weaker muscles, any restoration of the balance of power is short-lived. The weaker muscles may in this way be encouraged to reach their greatest power a little sooner than the stronger ones, but, in the course of natural activity after this, the stronger muscles will still continue to recover and the inequality will recur. Appreciation of these facts may be important in deciding whether or not to undertake tendon transplantation.

There is no standard answer to the problem of how long treatment devoted to muscle recovery should be continued. In most cases little further benefit accrues from treatment after nine or ten months; the final residue of gain in muscle power is usually developed in the course of ordinary activity. Occasionally, in a severely paralysed patient, or if the greatest possible effort is required from a muscle in the performance of an important function such as flexion of the elbow, it may be advisable to treat individual muscles for longer than nine months, but never to exceed a total of two years of treatment.

SUMMARY

  1. The results of a three-year study of recovery in 3,033 lower limb muscles and 1,905 upper limb muscles in 142 patients are presented.
  2. The rate of recovery of partly paralysed muscles is the same in all muscles and muscle groups in the lower or upper limb. Clinical differences in the ability of individual muscles to recover depend upon the proportions of their number that remain permanently paralysed.
  3. The rate of recovery is slowest in adults and most rapid in young children.
  4. The amount of further recovery to be expected in a muscle can be predicted from knowledge of its grade at any time after one month from the onset of the paralysis. Fourteen-fifteenths of the total amount of recovery takes place by the beginning of the twelfth month; with rare exceptions individual muscle recovery is complete after twenty-four months.
  5. Ninety per cent of muscles that are still completely paralysed after six months remain permanently paralysed.
  6. The prognosis of a completely paralysed muscle is related to the level of paralysis in muscles supplied by the same spinal segments.
  7. Deterioration in power in a muscle is uncommon and, when it occurs, is associated with the presence of the strong opposing force of antagonist muscles or of gravity.
  8. The application of these findings to the management of cases of paralytic acute anterior poliomyelitis is discussed.

I wish to acknowledge with thanks the help and guidance given to me by Mr H. J. Seddon, Director of Studies at the Institute of Orthopaedics, University of London, at which this work was undertaken under a grant from the Medical Research Council. The detailed figures, from which the results given here have been extracted, have been included in a thesis submitted to the University of Sheffield for the degree of Doctor of Medicine (1954).

REFERENCES

BROOKS, D. M. (1953): Nerve Conduction in Poliomyelitis. In The Spinal Cord. A Ciba Foundation Symposium Edited by J. L. Malcolm, J. A. B. Gray and G. E. W. Wostenholme, p. 280. London: J. & A. Churchill Ltd.

CARROLL, R. L. (1942): Rate and Amount of Improvement in Muscle Strength Following Infantile Paralysis. Physiotherapy Review, 22, 243.

COURTNEY, J. W. (1896): Acute Anterior Poliomyelitis. Boston Medical and Surgical Journal. 135, 617.

DANIELS, L., WILLIAMS, M., and WORTHINGHAM, C. (1947): Muscle Testing. Techniques of Manual Examination. Philadelphia and London: W. R. Saunders Company.

ELLIOTT, H. C. (1945): Studies on the Motor Cells of the Spinal Cord, iii. Position and Extent of Lesions in the Nuclear Pattern of Convalescent and Chronic Poliomyelitis Patients. American Journal of Pathology, 21, 87.

GREEN, W. T. (1949): The Management of Poliomyelitis: The Convalescent Stage. Poliomyelitis. Papers and Discussions Presented at the First International Poliomyelitis Conference, p. 165. Philadelphia: J. R. Lippincott Company.

GROSSIORD, A., and HUSSON, A. (1953): Le pronostic musculaire dans la poliomyélite. Éléments cliniques d'appréciation. Semaine des Hôpitaux de Paris, 29, 271.

HARRY, N. M. (1938): The Recovery Period in Anterior Poliomyelitis. British Medical Journal, i, 164.

KENDALL, H. O., and KENDALL, F. M. P. (1949): Muscles -- Testing and Function. Baltimore: Williams and Wilkins.

KNOWLEDEN, J., and SHARRARD, W. J, W. (1955): The Ineffectiveness of Splinting in the Treatment of Abductor Paralysis at the Shoulder. In Press.

LENHARD, R. E. (1943): The Results of Poliomyelitis in Baltimore. Journal of Bone and Joint Surgery, 25, 132.

MEDICAL RESEARCH COUNCIL (1942): War Memorandum No. 7. Aids to the Investigation of Peripheral Nerve Injuries. London: H.M. Stationery Office.

RUSSELL, W. R. (1952): Poliomyelitis. London: Edward Arnold & Co.

SEDDON, H. J. (1949): In Discussion of the Management of Poliomyelitis: The Convalescent Stage. Poliomyelitis. Papers and Discussions Presented at the First International Poliomyelitis Conference, p. 187. Philadelphia: J. B. Lippincott Company.

SHARRARD, W. J. W. (1953): Correlation Between Changes in the Spinal Cord and Muscle Paralysis in Poliomyelitis -- A Preliminary Report. Proceedings of the Royal Society of Medicine (Section of Orthopaedics), 46, 346.

SKINHØJ, E. (1949): Some Problems of Acute Anterior Poliomyelitis and its Sequelae. Copenhagen: Einar Munksgaard.

WATKINS, A. L. (1949): Progressive Disabilities in Poliomyelitis. Papers and Discussions Presented at the First International Poliomyelitis Conference, p. 142. Philadelphia: J. B. Lippincott Company.

WRIGHT, W. G. (1912): Muscle Training in the Treatment of Infantile Paralysis. Boston Medical and Surgical Journal, 167, 567.

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