Recovery following spinal cord injury.

Spinal cord injury (SCI) is one of the most devastating injuries an individuaL can sustain. Of paramount concern to patients and their families is what degree of return of function they can expect. This paper will review the general recovery of motor function as well as recovery of ambulation and other activities of daily living following a spinal cord injury.

In order to adequately assess recovery following spinal cord injury, it is necessary to have a common, reliable, and valid way of measuring recovery. A basic understanding of the anatomy of the spinal column, spinal cord, and motor and sensory nerves is needed to understand the components of the measurement tool.

The spinal cord consists of a central gray matter and surrounding white matter. The white matter contains the descending (motor) and ascending (sensory) tracts. These spinal tracts transmit information between the brain and body. The gray matter represents the neuronal cell bodies and is organized in a segmental manner with spinal nerves entering and exiting through the vertebral foramina. The roots are numbered and named according to their point of entry into or exit from the vertebral column. The roots receive sensory information from specific areas of skin called dermatomes. The term myotome refers to the group of muscles innervated by a specific root. Most roots, however, innervate more than one muscle, and most muscles have multilevel innervation.

In a spinal cord injury, transmission of motor and/or sensory information across the site of the lesion is interrupted or impaired. The cause of injury may be due to a vascular insult to the cord or to contusion or bruising of the cord, but violence or high velocity trauma such as motor vehicle accidents are the most common causes in the United States. The degree of motor and/or sensory loss is determined by the location and severity of the cord damage.

If the lesion is in the cervical segments of the cord, impairment of function in the arms, legs, trunk, and pelvic organs results. This is known as tetraplegia, although the term quadriplegia has also been used. Paraplegia refers to a lesion in the thoracic, lumbar, or sacral segments of the cord. Patients with paraplegia have normal arm function. Depending upon the level of the lesion, the trunk, legs, and pelvic organs may be affected. In addition to the general level of injury, i.e., tetraplegia or paraplegia, a specific neurologic level can often be identified by performing a detailed neurologic examination. The completeness of the injury can also be determined by neurologic examination. The term "incomplete" injury refers to partial preservation of sensory and/or motor function in the lowest sacral segments of the cord. A "complete" injury is one in which there is no preservation of function in the lowest sacral segments.

In 1982, the American Spinal Injury Association published guidelines for neurological classification of spinal cord injuries. The guidelines were revised in 1992, and the Standardsfor Neurological and Functional Classification of Spinal Cord Injury were subsequently endorsed by the International Medical Society of Paraplegia (ASIA, 1992). The ASIA standards represent the most valid, precise, and reliable data set to assess SCI and are used by the National Model System Spinal Cord Injury Database.

Prior to the publication of these guidelines, there was no universally accepted classification system for measuring the severity of SCI. Therefore, it was difficult to compare outcomes among different studies and it was difficult for physicians to accurately communicate among themselves when tracking patient progress. The system most commonly used prior to the acceptance of the ASIA standards was the Frankel score or the modified Frankel score (Franker, et al., 1969). In this system, patients were divided into five broad categories based on neurologic deficit. This system, however, was insensitive to patient changes within each category and utilized broad categories that were not well defined.

The neurological examination as recommended in the ASIA standards consists of both sensory and motor examinations. Sensation to both pin prick and light touch is assessed bilaterally at key points on the body representing each of the 28 dermatomes, which in turn represent the neural segments from C2 to S5 (see Figures 1 and 2). Sensation is assessed on a three-point scale with 0 designating absent sensation, 1 representing impaired sensation, and 2, normal sensation. Anal sensation is tested and sacral motor function is assessed by whether there is contraction of the external anal sphincter when the examiner's finger is inserted. Determination of anal sensation and contraction is necessary to determine the completeness of injury.

The motor examination is conducted by manual muscle testing of 10 key muscles on each side of the body. These muscles represent the myotomes for neural segments representing the arms (levels C5 through T1) and legs (levels L2 through S1). The strength of each of the 10 key muscles is graded on the standard 6-point scale (0=absent, 1=trace, 2=poor, 3=fair, 4=good, 5=normal).

Motor and sensory scores provide a quantitative representation of neurologic deficit. The ASIA Motor Score (AMS) is the sum of the strength grades for all 10 key muscles bilaterally. Thus, in an individual with no motor deficit, the total score would be 100. The sensory score is the sum of the sensory grades for each dermatome.

The neurological level of injury (NLI) is the lowest level of the spinal cord with normal sensory and motor function bilaterally. Because segments with normal function can vary by modality (sensory vs. motor function) and side of the body, up to four different segments can be identified: right-motor, right-sensory, left-motor, and left-sensory. Frequently, however, patients' neurological deficits are designated by a single motor level and a single sensory level.

Immediately following injury it is often difficult to perform an accurate neurological examination. The patient may be sedated, intoxicated, confused, or in pain. In addition, the patient may be undergoing acute medical or surgical stabilization. The obstacles to performing an accurate neurologic exam in the immediate postinjury period make it difficult to assess the effectiveness of early interventions such as surgery or drugs. The difficulty of performing an accurate examination in the acute postinjury period is, however, not a liability in obtaining predictors of recovery, since performing the neurological exam between 72 hours and 1 week following injury provides more accurate predictors of short-term recovery than when the exam is performed within the first 24 hours following injury.

When a patient undergoes sequential neurological examinations, the differences in motor and sensory scores between successive exams is representative of the recovery (or deterioration) that has occurred in the intervening time. By dividing the difference between scores by the number of intervening days, the change per day can be determined. Finally, by multiplying the change per day by 365, the annualized rate of change can be calculated. The annualized rate represents the rate of change during a particular interval that would have been expected if it were to have continued for 1 year. In general, recovery of sensation follows a pattern similar to that of motor recovery. Therefore, in this paper we will focus on motor recovery.

Recovery will be addressed in specific categories of patients. These findings are based on an 8-year prospective study funded by the National Institute on Disability and Rehabilitation Research and executed at Rancho Los Amigos Medical Center in Downey, California. This study constitutes the largest prospective investigation (over 500 cases) to determine the patterns of recovery conducted to date.

Bracken, et al. (1990) reported that recovery after spinal cord injury was significantly enhanced when methylprednisolone was administered within 8 hours following injury. Although the study was well designed, randomized, and controlled and included a large number of subjects, the results remain somewhat controversial. The differences in motor and sensory scores were significant but small. Additionally, when the randomized groups were closely examined, some biases which could affect outcomes were noted. Due to ethical and legal implications, it is no longer feasible to replicate the Bracken study or to test the effectiveness of other pharmaceutical interventions on recovery without including the administration of methylprednisolone. None of the patients in the Rancho study had received methylprednisolone following injury.

Complete Paraplegia

In a report on 142 individuals with complete paraplegia, none with an initial neurologic level (NLI) above T9 recovered any lower extremity (LE) function 1 year following injury. Although 38 percent of those with an NLI below T9 had some recovery of LE function, only 5 percent recovered sufficient hip and knee strength to ambulate using conventional orthoses and crutches. Additionally, all of the patients who regained ambulatory function had an NLI at or below T12. Four percent of individuals who were assessed as having complete injuries at admission converted to incomplete status. Half of these patients who underwent late conversion to incomplete status regained bowel and bladder control (Waters, Yakura, Adkins, & Sie, 1992).

Recovery Following Incomplete Paraplegia

Individuals with incomplete paraplegia demonstrated an average gain of 12 lower extremity motor score (LEMS) points 1 year following injury. Amount of recovery was not dependent upon NLI. Final motor status, however, was dependent upon NLI because individuals with NLI's above T12 had lower average initial LEMS's than those with NLI's at T12, who in turn had lower initial LEMS's than patients whose NLI's were below the T12 level. Seventy-six percent of the 54 individuals with incomplete paraplegia were able to ambulate in the community 1 year following injury (Waters, Adkins, Yakura, & Sie, 1994a).

Brown-Sequard injuries are a subset of incomplete injuries which occur when either the right or left side of the spinal cord is damaged. This type of spinal cord lesion results in diminished muscle strength and joint position sense on the same side of the body as the cord damage and loss of pin prick sensation on the side of the body opposite the cord lesion. These individuals usually have a favorable prognosis for recovery but few demonstrate the classic syndrome. Although these individuals frequently recover some motor function, significant residual spasticity usually interferes with function.

Recovery Following Complete Tetraplegia

Individuals with complete tetraplegia demonstrated an average AMS increase of nine points in the interval between admission and 1 year following injury. The initial AMS increased as the NLI's progressed from C4 to C8, but the average total point recovery did not vary. Thus, amount of recovery was independent of the initial NLI, but final absolute AMS was dependent on NLI. No individuals with complete tetraplegia were able to ambulate at followup (Waters, Adkins, Yakura, & Sie, 1993a).

Recovery Following Incomplete Tetraplegia

The motor recovery rates for individuals with incomplete tetraplegia do not differ significantly between the upper extremities and the lower extremities. Furthermore, recovery in the upper and lower extremities occurred concurrently. Forty-six percent of individuals with incomplete tetraplegia were able to ambulate in the community 1 year following injury.

Investigators have determined that individuals who are incomplete only by virtue of retained pin prick sensation sacrally have a better prognosis for lower extremity motor recovery than those who have only light touch sensation. Thus, sacral sensation is an important variable when predicting motor recovery.

Within this category of tetraplegia there are two specific incomplete syndromes with characteristic motor and sensory loss patterns. Anterior cord syndrome results in loss of motor function and pin prick sensation with retention of light touch sensation and joint position sense. Motor recovery in these individuals is similar to that in individuals with complete neurological injury. Central cord syndrome frequently occurs in older individuals as a result of hyperextension of the neck. In this syndrome, motor loss is more severe in the upper extremities compared to the lower extremities. These individuals often recover the ability to ambulate but retain weakness in their upper extremities (Waters, Adkins, Yakura, & Sie, 1994b).

Timing of Recovery

Graphic representation of annualized rates of recovery vs. time since injury have demonstrated that the rate of motor recovery rapidly decreases as time since injury increases (see chart). The greatest recovery occurs in the first 6 months following injury with a plateau in rate of recovery occurring at approximately 9 months postinjury.

[CHART 1 ILLUSTRATION OMITTED]

Functional Recovery

When a muscle is able to move a body part through the full range of motion against the force of gravity it has attained at least grade 3 of 5 and is considered functional. The strength of a muscle at 30 days was found to be predictive of recovery to a functional level (Waters, Adkins, Yakura, & Sie, 1995a). When muscles with a 30 day initial grade of zero and those with an initial grade of 1 or 2 were compared, a smaller percentage of 0 grade muscles recovered functional strength compared to muscles with an initial grade of 1 or 2. (Table 1). For example, 73-100 percent of individuals with incomplete injuries and initial muscle grades of 1 or 2 recovered to at least grade 3 by 1 year compared to 20 to 26 percent of those with grade muscles.

Table 1
Recovery to Grade 3/5 or Higher at One Year Following Injury
(% of muscles tested)

                         Strength at 30 Days

Injury Category         0/5         1/5 or 2/5

Incomplete Injuries     20-26%       73-100%
Complete Tetraplegia     4-22%           97%
Complete Paraplegia      4-8%         68-70%

Ditunno and colleagues (1991) found that recovery to at least grade 3/5 in the elbow flexors and extensors and the wrist extensors was more likely if the individual demonstrated voluntary motor function in those muscles 1 week following injury. They also reported that recovery of wrist extensors could be predicted from the initial strength of the elbow flexors (Ditunno, Sipski, Posuniak, Chen, Stass, & Herbison, 1987).

Recovery of a specific functional task is dependent upon the neurological recovery that an individual attains. Individuals with incomplete spinal injuries can have a wide range of sensory and motor function despite having the same neurological level of injury. For example, a patient with a C5 incomplete injury may have decreased motor function in the lower cervical myotomes but may have lower extremity muscles that are all present, although weak. This patient would have a more favorable prognosis for ambulation and other activities of daily living than another patient with an identical neurological level of C5 incomplete who had only spared sensation but no motor function. Because of this variance in function it is difficult to predict function based on level of injury in incomplete injuries.

Guidelines for expected level of function have, however, been developed for individuals with complete spinal cord injuries. Predictions about mobility, transfers, and self-care can be made when a patient's neurologic level of injury is known (Tables 2 and 3).

Table 2
Expected Function According to Level of Injury
Complete Tetraplegia

Neurologic Level   Mobility

C1-C3              Possible candidate for electric
                   wheelchair with portable
                   respirator and tongue switch/
                   breath control.

C4                 Electric wheelchair with chin
                   or tongue control.

C5                 Electric wheelchair with hand
                   control or possibly, manual
                   wheelchair with handrim
                   projections (pegs).

C6                 Manual wheelchair with
                   friction surface handrims.
                   May require electric wheelchair
                   for use in community.

C7                 Manual wheelchair may
                   require friction surface
                   handrims.

C8                 Manual wheelchair may
                   require friction surface
                   handrims.

T1                 Manual wheelchair
                   with standard handrims.

Neurologic Level    Transfers              Self-care

C1-C3               Dependent requiring    Dependent.
                    a lift.

C4                  Dependent requiring    Dependent.
                    a lift.

C5                  Dependent.             Assisted with light
                                           hygiene and self-feeding
                                           with proper equipment.

C6                  Independent with       Independent in UE
                    sliding board          activities with proper
                    and proper             equipment Independent
                    equipment              when assited with LE
                                           dressing and
                                           bowel/bladder management.

C7                  Independent with       Independent with proper
                    sliding board.         equipment.

C8                   Independent.          Independent.

T1                   Independent.          Independent.

Adapted from Adkins, R.H.: Spinal Cord Injury Capabilities and Consideration According to Level of Injury (unpublished).

Table 3
Expected Function according to Level of Injury
Complete Paraplegia

Neurologic level    Mobility             Transfer      Self-care

T1-T8               Manual wheelchair    Independent   Independent
                    with standard
                    handrim

T9-T12              Manual wheelchair    Independent   Independent
                    Some T12 may
                    ambulate

L1-L2               Manual wheelchair.   Independent   Independent
                    May be household or
                    limited community
                    ambulator with
                    crutches and
                    orthoses

L3-L5               May be community      Independent   Independent
                    ambulator with
                    proper equipment
                    and training.

Adapted form Adkins, R.H.: Spinal Cord Injury Capabilities and Considerations According to level of Injury (unpublished)

Ambulation

Restoration of walking remains one of the most important issues for patients. In general, a minority of individuals with SCI are able to resume walking following an injury. The level and completeness of injury does, however, influence the ability to ambulate. As previously stated, no patients with complete tetraplegia regained their ability to walk. Only 5 percent of those with complete paraplegia were able to walk 1 year following injury compared to 46 percent of those with incomplete tetraplegia and 76 percent of those with incomplete paraplegia (Waters, Adkins, Yakura, & Sie, 1994b).

The ASIA lower extremity motor score is also predictive of ability to walk. The total possible LEMS in an individual with no neurological deficit is 50 points. Individuals with a LEMS of 30 or more attained community ambulation status 1 year following injury. In contrast, those with a LEMS of 20 or less who were able to ambulate were able to do so only on a very limited basis. These individuals walked at much slower average velocities while demonstrating a greatly increased physiologic energy expenditure. Furthermore, early measurement of LEMS can also be used to predict ambulatory function. When the LEMS is determined at admission to the rehabilitation center and patients are grouped by level and completeness of injury, the proportion who are able to walk 1 year following injury increased as the initial LEMS increased.

Recovery Research

Using the methods outlined at the beginning of this report, neurological recovery has been studied in specific patient groups (individuals with spinal cord injury due to spondylosis, stab wounds, spinal cord infarct, or gun-shot wounds) to determine if unique recovery patterns can be differentiated based upon etiology of injury or treatment (Waters, Adkins, Yakura, & Sie, 1991, 1993b, 1995b, 1995c, submitted). The effect of anatomic pattern of injury on recovery has also been studied. The overall result of these investigations has been that the neurological level and completeness of injury at 30 days is the best predictor of recovery. Once the neurological status of the injury is known, the etiology and anatomic pattern of injury add no predictive power for recovery.

Summary

A detailed neurological examination performed approximately 1 month following injury currently provides the most reliable predictors for recovery of spinal cord injury. The majority of motor recovery that can be expected occurs within the first 6-9 months. At approximately 9 months the rate of recovery plateaus.

Acknowledgements

Research attributed to the authors and summarized in this manuscript was funded in part by National Institute on Disability and Rehabilitation Research Grants G008435028, H133G90115, and H133N00026.

References

[1.] American Spinal Injury Association. (1992). Standards for Neurological and Functional Classification of Spinal Cord Injury, Revised 1992. ASIA: Chicago

[2.] Bracken, M.B., Shepard, M.J., Collins, W.F., Holford, T.R., Baskin, D.S., Eisenberg, H.M., Flamm, E., Leo-Summers, L., Maroon, J.C., Marshall, L.F., Perot, P.L., Jr., Piepmeier, J., Sonntag, V.K.H., Wagner, F.C., Jr., Wilberger, J.L., Winn, H.R., & Young, W. (1990). A randomized controlled trial for methylprednisolone or naloxone in the treatment of acute spinal cord injury. Results of the Second National Acute Spinal Cord Injury Study. New England Journal of Medicine, 322, 1405-1411.

[3.] Ditunno, J.F., Sipski, M.L., Posuniak, E.A., Chen, Y.T., Stass, W.E., & Herbison, G.J. (1987). Wrist extensor recovery in traumatic quadriplegia. Archives of Physical Medicine and Rehabilitation, 68, 287-90.

[4.] Ditunno, J.F., Stover, S., Freed, M., & Ahn, Y. (1991). Motor recovery of the upper extremities in traumatic quadriplegia: a multicenter study. Journal of the American Paraplegia Society, 14, 94.

[5.] Frankel, H.L., Hancock, D.O., Hyslop, G., Melzak, J., Michaelis, L.S., Ungar, G.H., Vernon, J.D.S., & Walsh, J.J. (1969). The value of postural reduction in the initial management of closed injuries of the spine with paraplegia and tetraplegia. Paraplegia, 7, 179-92.

[6.] Waters, R.L., & Adkins, R.H. (1991). The effects of removal of bullet fragments retained in the spinal canal. A collaborative study by the National Spinal Cord Injury Model Systems. Spine, 16, 934-939.

[7.] Waters, R.L., Yakura, J.S., Adkins, R.H., & Sie, I. (1992). Recovery following complete paraplegia. Archives of Physical Medicine and Rehabilitation, 73, 784-789.

[8.] Waters, R.L., Adkins, R.H., Yakura, J.S., & Sie, I. (1993a). Motor and sensory recovery following complete tetraplegia. Archives of Physical Medicine and Rehabilitation, 74, 242-247.

[9.] Waters, R.L., Sie, I., Yakura, J., & Adkins, R. (1993b). Recovery following ischemic myelopathy. Journal of Trauma, 35, 837-839.

[10.] Waters, R.L., Adkins, R.H., Yakura, J.S., & Sie, I. (1994a). Motor and sensory recovery following incomplete paraplegia. Archives of Physical Medicine and Rehabilitation, 75, 67-72.

[11.] Waters, R.L., Adkins, R.H., Yakura, J.S., & Sie, I. (1994b). Motor and sensory recovery following incomplete tetraplegia. Archives of Physical Medicine and Rehabilitation, 75, 306-311.

[12.] Waters, R.L., Adkins, R.H., Yakura, J.S., & Sie, I. (1995a). Recovery Following Spinal Cord Injury: A Clincian's Handbook. Los Amigos Research and Education Institute, Inc., Downey, California.

[13.] Waters, R.L., Sie, I., Adkins, R.H., & Yakura J.S. (1995b). Motor recovery following spinal cord injury caused by stab wounds: a multicenter study. Paraplegia, 33, 98-101.

[14.] Waters, R.L., Sie, I., Adkins, R.H., & Yakura, J.S. (1995c). Injury pattern effect on motor recovery after traumatic spinal cord injury. Archives of Physical Medicine and Rehabilitation, 76, 440-443.

[15.] Waters, R.L., Adkins, R.H., Sie, I.H., & Yakura, J.S. (submitted). Motor recovery following spinal cord injury associated with cervical spondylosis: A collaborative study. Paraplegia.

Robert L. Waters, M. D. Ien H. Sie, M.S., PT. Rodney H. Adkins, Ph.D. Joy S. Yakura, M.S., P. T.

Dr. Waters is Chief Medical Officer, Rancho Los Amigos Medical Center and Clinical Professor of Orthopedic Surgery, University of Southern California, Downey, CA; Ms. Sie is Research Associate, Dr. Adkins is Co-Director, and Ms. Yakura is Research Associate at the Regional Spinal Cord Injury Care System of Southern California, Rancho Los Amigos Medical Center, Downey, California.