From the Archives
‘The effects of total transverse lesion of the spinal cord in man’. By James Collier, MD, B.Sc, FRCP. Assistant Physician (late Pathologist) to the National Hospital. Brain 1904; 27: 38–63.
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James Collier was appointed to the consultant staff of the National Hospital, London, in 1902. There, he started the weekly clinical demonstrations that soon became famous amongst students of neurology visiting Queen Square from throughout the world. He used ‘every histrionic trick of display, eloquence, gesture and emphasis ... despite a weakness for exaggeration, (Collier) possessed an uncanny clinical flair and diagnostic brilliance’ ... ‘the elegant phrases, falling to a whisper as, with the mannerisms of a magician, he disclosed the climax to the clinical story fascinated audiences at his Wednesday afternoon clinic’.
Writing in 1904, James Collier sets out a view on the mechanism of clinical deficits observed in total transverse lesions of the human spinal cord. His account predates (Sir) Charles Sherrington's great synthesis of the experimental data (The Integrative Actions of the Nervous System, 1906), and takes as its starting point observations previously published by H. Charlton Bastian, who had challenged the unqualified application of experimental observations to man, and considered that the tendon reflexes are permanently abolished after total spinal cord injury (On the symptomatology of total transverse lesions of the spinal cord, with special reference to the condition of the various reflexes. Medico-Chirurgical Transactions 1890; 73: 151–217).
Collier's emphasis is also on the evolution of tendon reflexes and electrical stimulation of the legs after spinal cord injury. He wants to make one point: ‘the argument of this paper is that as a result of total transverse lesion of the spinal cord, not only are the knee-jerks and other deep tendon reflexes permanently abolished in the region supplied by the caudal segment of the divided spinal cord, but in addition, the muscles waste ... and the sphincters lose their tone, the only sign of self-action remaining in the isolated part of the spinal cord being the occasional presence of certain of the skin reflexes in much reduced degree.’ Collier argues that loss of the tendon reflexes depends on isolation of the distal cord from higher centres rather than changes in the lumbo-sacral segment itself—as Sir William Gowers had proposed (Diseases of the Nervous System Vol. 1: 267). He demonstrates, for the first time, that the knee jerks can initially be elicited by intense Faradism, at least for a while. His case material, derived from the National Hospital, Queen Square and St Mary's Hospital in London, consists of wounds of the cord, fracture dislocations of the spine, spinal cord compression and examples of transverse myelitis. Many patients had been examined pathologically, and several were explored surgically.
Dealing first with the experimental literature, Collier concludes that isolation of the human spinal cord differs from the consequences of injury in cats and dogs, where transient depression of the reflexes is quickly followed by exaggerated reactions and retention of complex responses such as the scratch reflex. As Sherrington had already described in his Croonian lecture to the Royal Society, ‘autochthonicity’ is a much less characteristic feature of cord injury in primates (The mammalian spinal cord as an organ of reflex action. Philosphical Transactions 1898; 190: 45–186). Collier reminds readers that ‘the knee jerk has repeatedly been obtained in decapitated criminals, persisting for as long as 90 s after decapitation’. Thus, whilst the rate at which the features of independent spinal cord activity emerge is slower, in this (and, it must be said, in many other) respect(s) monkeys more closely resemble man than dogs. For Collier, the clinical literature is confused by the inclusion of cases having only partial cord injury. The only reliable criteria on which to base pathophysiological formulations are the direct demonstration of cord severance; a complete absence of myelinated fibres and axons traversing the lesion; and the cord shown to be entirely necrotic in transverse section. By comparison, cord atrophy is unreliable, and the demonstration of anaesthesia, complete flaccid paralysis and loss of the deep tendon reflexes merely reflects loss of function without necessarily informing on the structure of the cord. Thus, Case 6 (under the care of Dr Bastian and Sir Victor Horsley) had a complete physiological lesion but made an excellent recovery after removal of hydatid cysts compressing the mid-thoracic cord; much the same sequence is described for Case 13 who recovered from tuberculosis after surgical decompression by Sir Victor Horsley. Where degeneration has been complete, the subsequent development of spasticity and return of the knee jerks are explained by restoration of conduction through spinal cord regeneration.
Taking this material together, Collier describes the order in which the various features develop and may disappear. When the cord is injured gradually, motor paralysis and spasticity precede the subsequent ordered loss of ‘equilibratory’ sensation, sphincter control, pain and thermal sensibility, appreciation of touch, preservation of muscle tone, retention of the deep tendon reflexes, maintenance of muscle bulk, intact Faradic stimulation of the reflexes and preserved sphincter tone. These deficits advance from the extremities to the level of the lesion. In some cases, the evolution follows a more segmental distribution. Collier's observations on the bladder are that retention and reflex emptying indicate a partial lesion whereas constant dribbling from a small bladder is the rule after complete cord injury. That said, Cases 1, 2, 7 and 8 show acute retention in sudden complete lesions. At first, reflex evacuation of the bowel occurs in response to cold sacral skin stimulation, but with time the anal sphincter becomes patulous and constant escape occurs. Collier observes priapism (in Cases 3 and 12) but only in partial lesions, and abdominal distension (tympanitis) is also only an occasional finding.
When it occurs, recovery first manifests as return of the knee jerk and increased muscle tone. Sensation is re-established in the order touch, pain and then temperature. It starts in the lower sacral dermatomes, and is accompanied by gradual awareness of bladder distension or manipulation. The return of power is more apparent in the flexors than extensors, and starts with the ability to flex the toes. Return of the plantar response from extension to flexion is invariably the last feature to be recovered. Where regeneration is thought to have occurred, the degree of recovery is limited—restoration of the knee jerk and muscle tone, voluntary movement of the toes and awareness of passive joint movements being observed in the occasional patient.
But, with a mixed collection of case material, is the lesion complete or not? Rather little reliance can be placed on the presence of complete anaesthesia although, unrelieved, this does predict poor potential for recovery; and—for Collier—the presence of a hyperaesthetic zone at the border of the sensory level is unusual. With total lesions, the muscles are immediately flaccid, waste rapidly to resemble the appearances of anterior poliomyelitis (within 4 days from injury to death, in Case 1) and soon lose their Faradic excitability. Conversely, in the setting of incomplete lesions, wasting is minimal, muscle tone is increased and Faradism produces a slight response. The reflexes are lost and if these subsequently return it follows that the lesion cannot have been complete. ‘Strong and continued stimulation of the skin or nerves of the lower extremities has the effect of rousing the sleeping lumbo-sacral centres to such a degree of activity that their self-action is expressed by a temporary return of the deep tendon reflexes and in some cases by foot clonus’. Thus, stimulating the external (lateral) popliteal nerve with a needle electrode for 20 min and recording in the calf muscles shows muscle tone and restoration of the knee jerk for 5–15 min, if the lesion is of <3 days duration. These responses become progressively more difficult to elicit and no modulation can be achieved 10 days after injury. These opinions are backed up by the demonstration of spinal cord continuity in cases 11 and 12, coming to autopsy. In two cases, Collier considers that regeneration has occurred—return of the knee jerks then being anticipated by a transient response to Faradic stimulation. But, Case 4 is an example of early relief from spinal cord compression through removal (by Sir Victor Horsley) of a small meningioma (fibro-myxoma), with return to farm-labouring over the next few months; Case 2, who died from unrelated causes 16 months after an apparent total injury, recovered very limited functions and had, at autopsy, a ‘quill’ of cord continuity with fine fibres passing through the lesion that Collier considers to indicate regeneration.
A retained response to Faradism leads Collier to conclude that the lesion causing paralysis has spared the integrity of the lower cord, whereas the lack of such a response indicates that the lumbo-sacral enlargement and its roots are directly involved in the disease process. Thus, he disagrees with those who claim that the clinical features of total lesions depend on coincidental damage or consecutive structural changes to the lower motor neurones of the lumbosacral region of the cord. Collier reports that microscopic examination shows the ventral (anterior) cells to be normal: the only exception is that degeneration is to be expected in Clarke's nucleus and the equivalent sacral structures. The muscles do however show marked reduction in fibre size, although intrafusal fibres are spared, but with general retention of their transverse structure and with few changes in the nuclei, connective tissue and vascular appearances—in marked contrast to muscles where the nerve supply has directly been injured. Collier is dismissive of the opinion that isolation atrophy (tertiary degeneration) may reach the anterior horn cells and lower motor neurone in cases of total cord injury, thus accounting for loss of the deep tendon reflexes, or that degeneration in the posterior nerve roots and peripheral nerves might contribute to the clinical neurology of spinal cord injury. For him, the timing is all wrong and the core features—muscle wasting, loss of the tendon reflexes and lowering of Faradic excitability—are entirely the result of isolating the lumbo-sacral region of the cord from higher centres. But as for evidence, Collier provides rather little: of his 15 cases, only one includes any details of pathology in the isolated lumbo-sacral segment, and that is grossly abnormal through extensive hypertrophic pachymeningitis.
Ahead of his time, Collier sees the potential for repair, and the pragmatic need for early intervention, if structure and function are to be salvaged in the more favourable situations. But in declaring that total lesions have regenerated, on flimsy evidence either for complete nature of the original lesion or the re-growth of nerve fibres, and summarizing histological features that are not actually described, Collier is displaying the exaggeration and economy with scientific truth for which his Wednesday afternoon show at Queen Square was so notorious. Nonetheless, Collier believes that restoration of conduction through the lesion is the most parsimonious explanation for the recovery that is seen in certain cases and he has a message for clinical management that remains relevant a century later: ‘complete recovery has followed the removal of pressure where the signs of total abrogation of function of a transverse region of the cord have existed for as long as 7 days ... the recovery has been so rapid and complete as to make it certain that pressure may produce complete physiological abrogation for many days without necessarily entailing degeneration of the nerve elements ... onset of the flaccid state in compression paraplegia ... indicates that operative interference must be undertaken at once if it is to be of any avail, for the total physiological abrogation from compression signifies the presence of serious evascularisation, and the inevitable sequel of such ischaemia—irreparable degeneration—cannot be long delayed’.
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