In the early period after spinal cord injury (SCI), the care of SCI patients requires the cooperation of two teams: the surgical team and the rehabilitation team. 18 The surgical team is focused on preventing the progression of the neurologic deficit through the use of drugs, traction, and surgical correction of structural instability of the spine and associated structures. The focus of the rehabilitation team is to assess and maintain the multiple organ systems affected by SCI with the goal of restoring, substituting, and modifying function, and ultimately returning the patient to the community.
After patients with SCI survive the acute period and begin to mentally and emotionally process the nature of their injury, their primary question becomes “what will I be capable of and will I be able to walk?” Patients want to know whether they will be able to walk, work, perform self-care activities such as feed themselves, achieve sexual intimacy, have children, etc. In the past, clinicians that cared for SCI patients struggled to answer these questions. Fortunately, over the past several decades we have made significant strides in being able to accurately answer such questions. We are now capable of predicting with reasonable accuracy the long-term outcome for patients within a week of their initial injury. 20
This allows the SCI clinician to accurately convey information about prognosis. Patients and their families, based on accurate information, can then emotionally invest themselves in the pursuit of realistic goals. Patients and family members also need accurate information to begin the process of planning for postdischarge care and identifying the required resources.
In addition, physicians are often asked to justify the appropriateness of medical and rehabilitation interventions to third party payers based on expected outcomes. 20 To serve as effective patient advocates, SCI clinicians need to be familiar with the literature on neurologic recovery in SCI. The role of clinicians as advocates is likely to increase as society is forced to make difficult decisions regarding the allocation of medical resources.
In this article we review the literature regarding neurologic recovery in complete and incomplete spinal cord injuries as well as the prognosis for ambulation. In addition, we review the association of motor level to functional capacity. We then discuss new interventions that could possibly improve long-term rehabilitation outcomes.
Predicting Neurologic Recovery in Spinal Cord Injury
Definition of Complete Versus Incomplete Spinal Cord Injury
The first step in predicting motor recovery is to determine whether the patient is complete or incomplete. This is predicated on performing an accurate examination according to American Spinal Injury Association (ASIA) standards. 34,45 Using these criteria, SCIs are classified in descending order of severity from A through E (Table 1). According to ASIA criteria, an SCI is defined as complete when there is an absence of sensory and motor function in the lowest sacral segment (“sacral sparing”). This has been shown to be the most reliable and clinically useful definition. 60
In comparison, an incomplete injury is defined by the presence of sensory and/or motor function at the lowest sacral segment. Sacral sensation can include pinprick or light touch sensation at the anal mucocutaneous junction as well as deep anal sensation with digital examination. The test of motor function is the presence of voluntary contraction of the external anal sphincter on digital examination.
Other important terms include neurologic level of injury, motor level, sensory level, and zone of partial preservation. According to ASIA criteria, 34,45 neurologic level of injury is defined as the most caudal segment of the spinal cord with normal sensory and motor function on both sides of the body. In contrast, motor level refers to the most caudal segment of the spinal cord with normal motor function on both sides of the body. Normal motor function in this context means a motor grade of ≥3 with all the above motor levels being Grade 5. Sensory level is similarly defined as the most caudal segment with normal sensory function, light touch, and pinprick on both sides of the body. Zone of partial preservation refers to those dermatomes and myotomes caudal to the neurologic level of injury that remain partially innervated. The term is applicable only for complete injuries.
Timing of Examination
The next question involves when the prognostic examination should be performed. Stauffer cautioned against making a prognosis during spinal shock. 56 Spinal shock as defined by Stauffer, 56 however, is a vague clinical entity and has limited clinical utility. Indeed, it is rare for the patient to be admitted with the absence of all reflexes. The evolution of reflexes over several days after injury may be more relevant to prognosis than the term spinal shock and the accompanying presence or absence of reflexes on the day of injury. 38
Examinations performed in the emergency room are difficult and may lead to error, although for documentation purposes an examination as soon as possible after the injury may be important. It is our opinion, however, based on the results of earlier studies, that the 72-hour examination is superior to the first day examination for long-term prognostication. 5,44 This time frame has been used in several studies examining neurorecovery in SCI. 13,21,43 Prediction within the first week has become a rehabilitation imperative for purposes of justifying appropriate rehabilitation services to third party payers. 20
Another commonly used examination interval for predicting recovery is 1-month postinjury. 61–64 Historically, it tended to correspond more closely with the timing of admission to a rehabilitation facility, but recently managed care and medical reform have led to shorter lengths of stay for acute hospitalization. 23,25 Ideally, the clinician should base prognosis on examinations performed in the same time frame as the medical literature that the clinician chooses to use. 35,36
Complete Spinal Cord Injury
In complete tetraplegia there is little chance for functional motor recovery in the lower extremities if the patient remains motor and sensory complete >1 month postinjury. 62 Despite this fact, neurorecovery in the upper extremities remains important because this helps determine the level of functional independence with self-care. For a muscle to have “useful” motor function it must have at least Grade 3–5 motor strength (the ability to move a joint through a range of motion against gravity). 42,51–52,62,66,71
One approach to predicting recovery is to determine the likelihood of descent of the initial motor level. Unpublished data compiled by our center illustrate the association between having initial strength for a given motor level and the chances of gaining motor function at the next level (Figures 1 and 2). In a study by Ditunno et al, 16 it was observed that if motor strength was a Grade 2 to Grade 5 at a given motor level (C5 biceps) at 1 week postinjury, all patients gained functional strength (Grade ≥3 of 5) at the next motor level (C6 extensor carpi radialis). 16 Another recent study found that in complete tetraplegics there was a 70% to 85% likelihood of gaining at least one additional motor level. 21
Other studies have focused on the association between initial motor strength in a muscle and expected magnitude of recovery. Several studies in complete tetraplegia have found that more than 90% of muscles with Grade 1 of 5 or Grade 2 of 5 strength from 1 week to 1 month after injury will eventually recover to Grade ≥3 of 5 strength. 17,62 In contrast, muscles with Grade 0 of 5 strength 1 month after injury and located one neurologic level below the most caudal level having motor function regained Grade ≥3 of 5 strength in only 27% of cases at 1 year. 62 Muscles two levels below the most caudal level with motor function regained Grade ≥3 of 5 strength in only 1% of cases. Late conversion, i.e., >1 month postinjury, from complete to incomplete injury had little bearing on the ultimate motor recovery.
In another study on complete paraplegia using a 1-month baseline examination, Waters et al reported that in 73% (108 of 148) of patients, the neurologic level of injury did not change at 1 year. 61 Only two patients recovered >2 levels. None of the patients with an initial neurologic level above T9 regained any lower extremity motor function. In muscles with an initial Grade of 1 of 5 or 2 of 5, approximately 70% recovered to Grade 3 of 5 or greater at 1 year. In contrast, 3–7% of initially Grade 0 of 5 muscles progressed to Grade 3 of 5 at 1 year. In cases with initially “present” lower abdominal muscles, 26% of hip flexors recovered to Grade ≥3 of 5. Four percent (6 of 148) of the patients converted “late” to incomplete injuries. Three of six late converters regained bowel/bladder continence, and two of six ambulated with a reciprocal gait.
The majority of neurorecovery in complete patients occurs during the first 6 to 9 months. 17,61,62 Afterwards, the rate of improvement rapidly drops off with a plateau being reached 12 to 18 months postinjury with little additional improvement (Figure 3). 17,19,21,61,62
Incomplete Spinal Cord Injury
Incomplete injuries of the cervical spinal cord recover to a greater extent than complete injuries. A recent multicenter study compared the recovery of upper extremity strength in complete and incomplete tetraplegics. 21 Greater than 90% of incomplete injuries gained at least one additional motor level in the upper extremities compared with 70% to 85% of complete injuries. There is an excellent chance (92%) of recovery to ≥3–5 motor strength for initially 0–5 muscles if pinprick is spared at the same dermatome. 50
Waters et al prospectively studied motor and sensory recovery in incomplete tetraplegia and incomplete paraplegia using a 1-month baseline examination in one center. 63,64 Using ASIA criteria they reported that the magnitude and rate of recovery are relatively constant regardless of the initial neurologic level of injury. ASIA criteria identify five key muscles in the upper extremity and five key muscles in the lower extremity. Each muscle is graded from 1 to 5 for the right and left so that the maximum motor score is 50 for the lower extremities.
In the majority of incomplete tetraplegics and paraplegics, there was an approximately 12- to 14-point increase in lower extremity motor scores during the first year and minimal improvement during the second year using the 50-point scale. The exception was incomplete tetraplegics without sharp–dull discrimination who failed to demonstrate any lower extremity motor recovery. In tetraplegics upper extremity motor scores improved 11 points by 1 year with little additional improvement by 2 years.
In incomplete paraplegia 85% of muscles that were Grade 1–5 or 2–5 at 1 month recovered to ≥3–5 by 1 year. In comparison, of 212 muscles that were Grade 0–5 at 1 month, 55% (117 of 212) recovered some volitional control, but only 26% (55 of 212) recovered “motor useful” (≥3–5) function. The study on incomplete tetraplegia found similar magnitudes of neurorecovery. 64 In both incomplete paraplegia and tetraplegia, the majority of improvement occurred within the first 6 to 9 months and a plateau was reached by 12 months (Figure 3). 63–64
The anterior spinal syndrome predominantly affects the spinothalamic tracts and corticospinal tracts while sparing the posterior columns. Motor recovery is thought to be significantly less in these patients in comparison with other incomplete patients. 12,26 Central cord syndrome is characterized by disproportionately more motor impairment of the upper than the lower extremities. Prior studies have reported that 57% to 86% of patients with this syndrome will independently ambulate. 2,46 Penrod et al 47 assessed the impact of age in central cord syndrome and noted that 97% (29 of 30) of patients younger than 50 years ambulated compared with 41% (7 of 17) of patients older than 50 years. Foo 27 found that in central cord syndrome due to cervical spondylosis, only 31% of patients ambulated, with the mean age of study subjects being 65 years. The Brown-Sequard syndrome produces relatively greater ipsilateral proprioceptive and motor loss and contralateral loss of sensitivity to pin and temperature. The prognosis is also favorable with this syndrome, and almost all patients will ambulate successfully. 2,47,57 It has been theorized that axons in the contralateral cord may facilitate recovery. 41 Motor return also tends to occur in a proximal-to-distal pattern with extension returning before flexion. 41
Prognosis for Ambulation
The motor requirements for community ambulation have been previously defined. 13,33 To be a community ambulator, one must be able to walk reasonable distances both in and out of the home unassisted by another person. It is thought that to be an effective community ambulator, the person with SCI must have Grade ≥3–5 strength in the hip flexors on one side and Grade ≥3–5 or greater strength in the quadriceps on the other side. This would enable the individual to ambulate using one short leg brace with a fixed ankle unit set in a few degrees of dorsiflexion and one long leg brace with a similarly fixed ankle unit and a locked knee joint. Intact proprioception also has to be present. Using the 50-point lower extremity motor scale, prognosis for ambulation can be predicted for various categories of SCI (Table 2).
It has been clearly established that patients with complete spinal cord injuries rarely walk. 44 In one study on complete paraplegics, 5% (7 of 148) of complete injuries at 1 month were eventually able to reciprocally ambulate using conventional orthoses and crutches. 61 Two of these patients were late converters to incomplete status. In a similar study on 61 complete tetraplegics, 90% had no return of volitional lower extremity function and no patients were reported to ambulate. 62
In their article on recovery in incomplete paraplegia, Waters et al reported that 76% (41 of 54) of incomplete patients eventually became community ambulators: 38 by 1 year and three by 2 years. 63 A distinction was not made between the incomplete ASIA grades (B–E). All 29 patients with an initial (1-month) lower extremity motor score of ≥10 points ambulated by 1 year. Seventy percent (7 of 10) of patients with an initial motor score between 1 and 9 ambulated by 1 year. Thirty-three percent (5 of 15) of patients with an initial motor score equaling 0 ambulated by 1 year. Furthermore, all patients with an initial hip flexor or knee extensor Grade ≥2–5 ambulated in the community by 1 year. Similarly, Crozier et al reported that all patients with an initial quadriceps strength of at least Grade 2–5 who attained a grade of ≥3–5 in at least one quadriceps by 2 months postinjury were able to ambulate functionally at follow-up. 13
In comparison with incomplete paraplegics, incomplete tetraplegics are less likely to ambulate. Waters et al found that only 46% of incomplete tetraplegics (vs. 76% of incomplete paraplegics) were community ambulators 1 year postinjury 64; they attributed this to the fact that upper extremity strength is often severely compromised in the tetraplegic and therefore insufficient to enable crutch-assisted ambulation. Burns et al also focused on the recovery of ambulation in motor incomplete tetraplegic patients. 7 Ninety-one percent (30 of 33) of ASIA C patients younger than 50 years of age ambulated compared with 42% (13 of 31) of ASIA C patients age 50 or older. All (41 of 41) ASIA D patients ambulated regardless of age. Foo 27 focused on SCI related to cervical spondylosis. Thirty-one percent (10 of 32) of the incomplete patients became independent ambulators; however, the average age of study patients was 65 years. 27 Both the studies by Burns et al 7 and Foo 27 emphasize the impact of age on ultimate prognosis.
A unique subcategory of incomplete injuries is the individuals with preserved sensation but no motor function (“motor complete”). Maynard et al 44 found that 44% (8 of 18) of initially motor complete (preserved sensation but no motor function) patients ambulated. Crozier et al 12 later demonstrated that the preservation of pinprick significantly impacts the prognosis for ambulation in motor complete patients. Using a 72-hour baseline examination, 89% of patients with pinprick ambulated compared with 11% with preserved light touch but no pinprick. This is thought to be explained by the proximity of the spinothalamic tracts, which mediate pinprick, to the lateral corticospinal tracts.
Prediction of Functional Capacity Based on Neurologic Level
The first attempt to relate functional capacity to level of injury was based on clinical observation and published in 1955 by Long and Lawton. 42 Their astute observations 42 have stood the test of time and have served as a guide for estimating functional capacity based on the neurologic examination and level for close to 50 years (Table 3). Recent textbooks have used a similar outline with minor revisions. 28,55 Other investigators have also examined the impact of injury level on function. 66,73 The Consortium for Spinal Cord Medicine recently published an excellent set of clinical practice guidelines on expected outcomes after traumatic SCI. 11 For this discussion, level of injury refers to motor level. It has been previously shown that motor level correlates with self-care function and is superior to the single neurologic level. 43 Motor level and neurologic level were previously defined above. It is also assumed for the sake of discussion that patients are complete and sharply demarcated at their described motor level.
C1–C4 patients are dependent for activities of daily living (ADLs), bed mobility, and transfers. They can often use a motorized wheelchair with specialized control mechanisms such as sip-and-puff. C1–C3 patients are also usually permanently dependent on mechanical ventilation. 40,69 C5 patients have active elbow flexion and can perform some simple ADLs with setup and special hand devices. This group of patients is otherwise dependent on an attendant for ADLs and transfers. They are unable to roll over or come to a sitting position in bed without additional adaptive devices. They can use a motorized wheelchair with hand controls, but they are unable to propel themselves in a manual wheelchair.
C6 patients have full innervation of the rotator cuff musculature and added shoulder stability. More importantly, active wrist extension is possible using the extensor carpi radialis. Active wrist extension is accompanied by passive finger flexion and opposition of the second digit with the thumb. This passive grip is referred to as a tenodesis grip and can be developed with appropriate occupational therapy to grasp and manipulate objects. Tenodesis grip can be strengthened using a wrist-driven flexor-hinge orthosis. Nevertheless, most of these patients still require assistance for ADLs, bed mobility, and transfers. Wheelchair propulsion is also possible for short distances on smooth, level surfaces. Hand rim projections (knobs) can facilitate this.
C7 patients gain functional strength in the triceps. The ability to forcefully extend the elbow allows the patient to lift their body weight. These patients can roll over, sit up in bed, and move about in the sitting position. Motivated patients can also transfer independently. Some assistance may still be required for toileting and dressing activities, particularly for the lower extremities. Eating can be done independently except for cutting. Independent wheelchair propulsion is possible for long distances on smooth surfaces.
C8 and T1 patients gain increasingly greater intrinsic hand function. This results in improved grasp strength and dexterity. This patient should be independent with bed mobility and transfers. Individuals with levels of C8 and below should also be independent with ADLs. Patients with injuries below T1 are at a minimum independent at wheelchair level. Prospects for meaningful ambulation depend on the variables discussed above. Sitting balance progressively improves with lower thoracic levels.
New Rehabilitation Interventions
In the near future, it can be expected that there will be an increasing number of pharmacologic interventions directed at improving the long-term outcome from spinal cord injury. 39 For the purposes of objectively evaluating new treatment interventions, more precise outcome measures will be needed. Currently, the Functional Independence Measure defines community ambulation as the ability to ambulate 150 ft but does not distinguish between devices so that a person ambulating with a walker and two long leg braces is rated the same as another person ambulating with one cane and no braces. Although the Functional Independence Measure may have value for describing extent of independence or conversely the amount of assistance required, it will have limited value in clinical trials requiring a more precise measure of walking ability. New outcome measures for walking, such as the Walking Index for Spinal Cord Injury and subscales of the Spinal Cord Injury Independence Measure, may provide more accurate measures of improvement in walking. 9,22
Within the past 15 years, studies have been published on agents directed at minimizing secondary injury from SCI, facilitating neurorecovery, and enhancing function of compromised axons. Methylprednisolone in the acute setting has been accepted as the standard of care in the United States and is thought to improve long-term recovery. 3,4 There has also been preliminary evidence suggesting that GM-1 ganglioside might improve neurorecovery. 30,59 It is thought to work by augmenting axonal sprouting. Results of a multicenter study to confirm its efficacy are pending publication. 31 4-Aminopyridine is being evaluated as a potential intervention for chronic spinal cord injury. 32,48,49,53,54 It is a voltage-gated, fast potassium channel blocker that is believed to improve axonal conduction by facilitating the propagation of action potentials in demyelinated nerve fibers. The interaction of these agents with specific therapy programs and their role in optimizing functional independence remain to be elucidated. In addition, regeneration research continues in animals, and trials of cell transplantation are underway in humans. 70
Another exciting, new intervention that directly involves physical retraining is body weight support gait training. The explanation for how this might work is based on the theoretical existence of a secondary central pattern generator in the lumbar spinal cord. Based on animal and human work, it has been postulated that training this pattern generator with body weight support might facilitate the recovery of walking. 14,15,24,39,67,68 Currently, a National Institutes of Health funded multicenter study is being conducted to evaluate its potential efficacy in humans. In the future, methods that use the concept of activity-dependent neuroplasticity will most likely play an increasing role in the rehabilitation of SCI patients.
The role of electrical stimulation in gait training also needs to be elucidated. 39 Functional neuromuscular stimulation (FNS) is defined as the use of electrical stimulation to activate paralyzed or paretic muscles in precise sequence and intensity to assist in the performance of ADLs. 10 Devices that provide FNS are called neuroprostheses.
A processor controls the delivery of electrical stimulation to targeted muscles. Open loop systems do not receive input from the environment and therefore do not correct for differences between actual and intended movements. In closed loop systems the processor receives some form of input from the environment and adjusts output accordingly. The majority of the current clinical devices are open loop.
Another important variable is the mechanism of delivery for electrical current. Current can be applied externally or internally through implantation. With implantation there is the risk of infection, but selectivity and efficiency of activation are improved. Also, current requirements are significantly reduced. One implantable device approved by the Food and Drug Administration is the Freehand System (NeuroControl Corporation in Cleveland, OH).
Clinically, hand neuroprosthesis devices are being predominantly used in C5 and C6 patients to provide grasp using either a lateral pinch or palmar prehension. The applicability in C4 and above patients is currently limited secondarily to an inability to move their arms in space. In C7 and below patients, grasp can usually be augmented by alternative procedures such as tendon transfers.
Functional neuromuscular stimulation is also being used for standing and walking in SCI. One such device that uses surface stimulation and that has been approved by the Food and Drug Administration is the Parastep System (Sigmedics, Inc., Northfield, IL). It uses a walker in conjunction with FNS and requires some upper extremity function. Constant stimulation of the antigravity muscles can lead to fatigue and limits distance walked. Currently, gait with FNS remains inefficient with significantly higher energy consumption in comparison with normal gait. Researchers are also developing implantable devices. 10
The role of electric stimulation in managing bowel and bladder dysfunction as well as the collection of semen for artificial insemination are described in an accompanying article in this issue of Spine. 6 Research also continues on other applications of electrical stimulation such as the treatment of pressure ulcers and pain. 1,8,29,37,58,72
In summary, advances in pharmacologic treatment, training, and FNS, along with the potential for future regeneration strategies, have led to increased optimism and excitement regarding the prospects for future successful rehabilitation interventions.
Over the past two decades, landmark studies have been published on the natural history of neurorecovery after SCI. As clinicians, we can now predict long-term outcome for most SCIs with a reasonable degree of confidence. This will become increasingly important as third-party payers continue their efforts to efficiently ration medical services. Furthermore, current research gives rise to the hope that in the near future clinicians will be actively intervening in an attempt to alter and augment natural recovery. As this comes to fruition, functional outcomes and quality of life for SCI patients should improve.
- Predicting recovery and functional outcome after SCI should be based on accurate neurologic examinations during the initial 4 weeks and is essential for the planning of rehabilitation.
- Improvement in the arms and hands can be predicted for patients with complete and incomplete tetraplegia within 1 week of injury.
- Walking function based on sensory and motor examinations within 2–4 weeks after injury can be predicted in patients with incomplete tetraplegia and paraplegia.
- Improvement in upper extremity and walking function is likely to improve in the near future based on promising results in drug and physical training trials.
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