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Review Article the Applied Neuropathology of Human Spinal Spinal Cord (1999) 37, 79 ± 88 ã 1999 International Medical Society of Paraplegia All rights reserved 1362 ± 4393/99 $12.00 http://www.stockton-press.co.uk/sc Review Article The applied neuropathology of human spinal cord injury BA Kakulas*,1 1Department of Neuropathology, Royal Perth Hospital, Queen Elizabeth II Medical Centre, Australia Keywords: spinal cord injury; neuropathology; future directions Introduction The timeliness of a review of the neuropathology of Wolman3 observed that SCI was a modern disease human spinal cord injury (SCI) centres on the related to industrialisation with the advent of the increasing interest in central axonal regeneration in railways and motor transport. Many of his observa- the search for a `cure' of spinal paralysis. Neuropathol- tions hold true today including the rarity of ogy contributes to this end by describing the nature of compressive eects attributable to epidural, subdural the disorder to be cured. More broadly a knowledge of and subarachnoid haemorrhages. The lack of equiva- the neuropathology underlying SCI is essential also for lence between experimental injuries which are precise the clinician responsible for management of the patient and human SCI lesions which are diuse remains as well as the neuroscientist working on SCI. There has topical. He points out that human SCI has multiple been spectacular progress in neurobiology in recent morphologies; contusions, lacerations, haemorrhages, years with CNS repair and regeneration now reported maceration, extensive cone-shaped necroses and cysts by many centres. However, in order for these are all described. Of special interest, because of our discoveries to be applied to human SCI an apprecia- own studies, is his observation that the spinal column tion of the neuropathology is required. The neurobiol- may be injured with the spinal cord remaining intact ogist must be aware of the nature of the condition to and the reverse. The distinction between blunt and be cured for the research to be relevant. Furthermore, penetrating injuries is to the point. He describes the before the experimental ®ndings may be applied to the susceptibility of the cervical spine to injury when patient it must be shown that the reactions to injury aected by degenerative osteoarthrosis which is also a are comparable in each. An outline of recent advances prevailing theme even today. He summarises the in the neurobiology of experimental SCI is therefore literature concerned with nerve root regenerations as included in this review in order to bridge the gap a late phenomenon these being derived mainly from the between human SCI and the experimental models. posterior horns and root ganglia. The reader is referred Most importantly the insight provided by the complex- to these articles for a fuller account of his studies.3±5 ity of the problem of ®nding a cure serves to inform Of the several aspects of human SCI which remain those waiting for this to occur to be realistic in their controversial, the mechanism of injury requires expectations. discussion especially in view of recent observations concerning `discomplete' cases and the phenomenon of Historical review `secondary' or continuing damage. Braakman and Penning7 correctly point out that mechanical compres- There are several excellent reviews of the neuropathol- sion due to displacement of the vertebrae which may ogy of human SCI. Ancient texts which refer to spinal be momentary is the principal cause of spinal cord injury such as the Edwin Smith Surgical Papyrus damage. They also emphasise that radiographic C3000-2500 BC and the writings of Hippocrates, examination may be normal in 50% of cases with Celsus, Ambrose Pare, Paulus of Aegina and Galen cervical cord lesions. The rarity of extradural or are quoted by J Trevor Hughes1 in his monograph on intramedullary haematomas which would require spinal cord pathology. He and others provide excellent surgical decompression is also documented and they summaries of the 19th and 20th century literature.2±6 question the value of decompressive laminectomy. Sir A few of the highlights follow. Ludwig Guttmann6 in his monumental work also subscribes to the view that the cord is damaged immediately by acute compression with the destruction *Correspondence: BA Kakulas, Department of Neuropathology, Royal Perth Hospital, Australian Neuromuscular Research of nervous tissue elements and their blood supply at Institute, Queen Elizabeth II Medical Centre, Australia the time of impact. Sir Ludwig was also one of the Neuropathology of SCI BA Kakulas 80 ®rst to consider the natural history of SCI with acute, were clinically incomplete and neurological exam- intermediate and late stages recognised. He noted that ination showed the central cord syndrome of late deterioration requires a pathological explanation. Schneider et al.10 These patients had no grey In addition to his excellent synopsis of the early matter changes at autopsy but axonal disruption literature, Jellinger2 draws on his own extensive was present in the surrounding white matter experience of SCI in his review of SCI. His approach especially in the lateral columns. These authors is classic, dealing with open and closed injuries conclude that `these ®ndings suggest that in a separately thus underlining the distinction between subset of human cord injury the cord lesion penetrating (war) injuries and the industrial and motor present is primarily a focal damage to axon- vehicle accidents of civil life. Concerning the mechan- myelin units, largely con®ned to white matter ism of injury these are grouped conventionally into; regions of the cord. This may be considered a focal (1) ¯exion and (2) de¯exion, ie hyperextension or axonal loss from white matter damage and may be dorsi¯exion injuries, (3) vertical compression, (4) similar, except in distribution, to the disseminated rotation, (5) injuries with combined mechanisms. He axonal loss seen in head injury'.9 These patients was also one of the ®rst to describe the dierent eects were mostly elderly and had relatively minor of each type of injury on the anterior and posterior injuries which were aggravated by the presence of longitudinal ligaments and recognises primary damage advanced degenerative arthritis of the cervical of the spinal roots and nerve root regenerations in the spine. Martin et al11 also reported a case of chronic lesions. He also draws attention to the modern central cord syndrome at C3-4 with similar white concept of primary and secondary damage and agrees matter changes demonstrated by pre and post- that compressive or space-taking eects of haemor- mortem MRI as well as histopathologically. In rhages, epidural or subdural which may require their patient recent necrosis was present in the surgical decompression are rare. Late sequelae and right anterior horn at C4-5. complications are discussed including local and remote eects in the cord. However, he does not clearly Leditschke et al12 described 100 fatal SCI cases distinguish between residual cysts and syringomyelia, a involving motor vehicles. Sixty showed damage to the matter which has recently been considered in relation- cervical spine, involving bony or disc damage in 31 ship to spinal stenosis.8 and focal haemorrhages in another 29. In eight cases, In his account of the mechanism of injury, Trevor pre-mortem radiology failed to detect lesions which Hughes1 considers that malalignment following injury were found by postmortem radiology and pathological narrows the spinal canal so that the spinal cord is examination. The initial radiological examination pinched between the lower vertebral body and the `missed' many laterally placed fractures and small neural arch of the vertebra above. He also refers to the chip fractures. absence of radiological evidence of injury in many There is considerable interest in spinal cord injuries cases especially in `rotation and ¯exion' injury. in Japan. Kinoshita13 published autopsies on 31 Among the more recent publications of human SCI patients performed between 1957 and 1987. Nine of pathology, one of the most important is that of Bunge his patients were elderly with rigid spines. The et al.9 These authors give details of 22 cases of spinal susceptibility of older people to hyperextension cord injury with MRI and pathological correlation. injuries is further described in a later report.14 Cross The patients were aged 16 ± 80 years with survival 3 h sections showed total absence of cord parenchyma at to 22 years. Sixteen of the 22 cases were cervical. They the level of injury. Haemorrhagic necrosis is demon- were classi®ed into four groups: strated in others.13 Ito et al15 describe eight patients who died following SCI. In one of these, neurological (1) Contusion cyst deterioration continued for 43 h following injury. At Five of their 22 cases showed this type of injury. autopsy an unusually extensive longitudinal spreading The authors considered this lesion to be compar- pencil lesion was found to extend from the medulla to able to the experimental animal models. T5. (2) Cord maceration Taylor16 has made an extensive study of vertebral Seven of their 22 cases showed massive compres- fractures by a delicate dissection technique in which sion after closed injury, the cord being lacerated the cervical spine is sectioned vertically at 2 mm and severley distorted. In three of these, fragments intervals in the coronal plane. He has also shown of remaining CNS parenchyma was found suggest- that in a large number of patients, small `tear drop' ing that a small number of central nerve ®bres may fractures of the vertebral body and small fractures of occasionally maintain their continuity. the zygapophyseal (facet) joints are not visible in X- (3) Cord laceration rays. He emphasises the frequency of pulposus Six of 22 patients showed this type of lesion which haemorrhages and tears of the annulus.17 Taylor's were due to gunshot wounds. observations are of great medico-legal importance (4) Solidcordinjury especially in litigation concerning `whiplash' injuries Four cases fell into this group.
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