6.2 Spinal cord injury severity measures
1 Evolution of classification systems
The anatomical and physiological complexity of the spinal cord is daunting and a perfect grading system for neurological function following human spinal cord injury (SCI) is almost certainly unobtainable. Developing a sensitive scale which precisely, accurately, and reliably describes the innumerable functions of this complex structure in a fashion that can both track or even predict neurological recovery is thus a monumental challenge. However, considerable advances have occurred over the past two decades in the development of valid, objective assessment techniques to measure changes in spinal cord function in the setting of injury or disease [3].
Classification systems for SCI seem as old as medicine itself: perhaps the first classification scheme came from Imhotep, physician to Pharaoh Zoser III of Egypt. Imhotep classified the injuries in poetic fashion as “a disease I shall treat”, “a disease I shall fight”, or “a disease which cannot be treated” [1]. Not surprisingly, this subjective system did not stand the test of time. Another historic advance came from the great physician Galen, whose contributions to medicine seem under-recognized by the mere naming of a vein in his honor. He is said to be the first to discriminate between different neurological levels of injury [1].
2 Current spinal cord injury classification systems
Frankel Grade
The first widely accepted classification scheme to assess neurological function following SCI was not described until 1967 when Frankel published his classic work [2]. Frankel applied his simple and convenient 5-point scale to patients undergoing postural reduction treated at the National Spinal Injuries Center at the Stoke Mandeville Hospital. Patients were classified “arbitrarily” as Complete (A), Sensory only (B), Motor Useless (C), Motor Useful (D), or Recovery (E). This work has had considerable influence and its general framework lives on in more modern classification schemes. Although insensitive, it provided a n easy scheme for classifying patients based on obvious and easily assessed aspects of neurological function. A major short-coming of this scale, however, is the subjectivity inherent in judging what constitutes “useful”. This scale also fails to recognize laterality and the independence with which motor and sensory function can be lost. Furthermore, scores of C and D have a ceiling effect, or discontinuity, whereby disproportionately few patients improve beyond these scores [3]. This scale does, however, seem remarkably forward-thinking when today’s emphasis on the functional significance is considered.
Lucas Neuro Trauma Motor Index
The next influential scale came in 1979 from Lucas and Ducker [1]. Their system was based on both the bony level of injury and corresponding motor function. Their scale was unique in that it subdivided SCI into two types of complete lesions (neurology consistent with the bony level or caudal to it) and three types of partial lesions. Their emphasis on statistical analysis (using their motor index initial, motor index current, and recovery rate) is to be commended, however their scheme was not widely used largely because it ignores sensory function.
Tator Sunnybrook Scale
The Sunnybrook Scale, devised by Charles Tator [3] in 1982, was the next major attempt to classify neurological function following SCI. Born out of a desire to produce “a more comprehensive assessment of recovery factors”, it was essentially a modification of the Frankel scale, which subdivided C and D scores. It was thus a more sensitive ten point scale that facilitated more independent scoring of motor and sensory deficits. It also emphasized that the level of injury should be defined as the most dist a l level of intact neurological function as opposed to the most proximal damaged level, or the bony level of injury; this convention persists to this day.
American Spinal Injury Association Score
The 1980’s saw a giant leap forward for this field. The first NASCIS trial [4] and the American Spinal Injury Association (ASIA) grading system [5] ushered in a new era of precision, complexity, and rigor in neurological assessment. The scoring system used in the first NASCIS trial, published in 1984, was developed during a 2-year feasibility study. They utilized approved examiners and assessed motor function, pinprick, and light touch, producing both an expanded score and a simpler five-point scale. The motor assessment applied the Royal Medical Research Council (MRC) of Great Britain Grading Scale to 14 muscle groups chosen for functional importance, representation of spinal cord segments, and ease of examination. The sensory testing was conducted from C2 to S5, and graded as normal, decreased, or absent.
The ASIA scale is similar, and has become the most widely accepted and used scale. This scale, first published in 1982 [5] has become an international standard endorsed by the International Medical Society of Paraplegia (IMSOP). Furthermore, it has undergone numerous revisions over the years [6] and is alternatively known as the International Standard for Neurological Classification of Spinal Cord Injury. The ASIA/IMSOP scale (referred to here as the ASIA scale for brevity) tests five key muscles in each extremity, each scored out of five, thus totaling 100. It also allows for optional testing of the diaphragm, deltoids, abdominals, medial hamstrings, and hip adductors. Here sensory testing is also completed for pin prick and light touch and graded in the same fashion as the NASCIS I trial, allowing the generation of scores for each out of 112. Position sense and awareness of deep pressure/pain are also included as optional. Also similar to the NASCIS I scale, ASIA scores can be presented in simplified form via the ASIA Impairment Scale, or AIS. The AIS is essentially a modernization of the Frankel scale and bears the same form. Here A remains a complete injury and E remains normal neurological function. Intervening scores have been made more objective, with muscle power grade of 3 used to discriminate between them, but despite increased objectivity a ceiling effect continues to plague C and D scores [3].
Modified Benzel Classification System
While these “modern” scales have been a tremendous advance, they are far from perfect. Indeed, they are markedly more sensitive than their predecessors, allowing for independent motor and sensory scoring as well as delineation of sidedness. Their simplified forms allow for simplified grading, facile communication, and easy comparison to older scales. They have some drawbacks, however. Their complexity makes them time-consuming and mandate performance by specially trained personnel. As well, many aspects of spinal cord physiology remain neglected such as bowel and bladder function.
The Modified Benzel Classification system [7, 8] is a scale which attempted to address some of these deficits. It is the most recently proposed classification system and it was used in the GM-1 ganglioside trial [9]. This scale has seven grades owing to a sub-division of ASIA D into three different grades. Furthermore, this scale additionally assesses walking and sphincter function. Though a step in the right direction, this grading system has not been fully validated and cannot be applied immediately following injury when a patient is unable to ambulate [3].
Functional outcomes measures
Recent years have seen a shift across the medical literature, placing a new emphasis on quality of life measures, recognizing it as perhaps the most important health outcome. Though Ben zel’s effort is a n exception, quality of life scales have largely been used in parallel with the neurological scales to this point. The Functional Independence Measure (FIM) has been perhaps most widely used in the SCI literature. It was developed from the Uniform National Data System for Medical Rehabilitation [10] and its scoring system evaluates areas of self-care, sphincter control, mobility, locomotion, and communication. Grossly classifications are made as independent or dependent, and it was largely designed to determine burden of care. Designed for widespread application to all rehabilitation patients, many felt the need to design a scale more relevant to those with SCI. In response, Catz et al published the Spinal Cord Independence Measure (SCIM) in 2001 [11]. The SCIM covers three areas of function: self-care (score range 0 ± 20), respiration and sphincter management (0 ± 40), and mobility (0 ± 40) and has indeed demonstrated more sensitivity to functional changes in SCI patients than the FIM. It has subsequently been revised to increase interobserver reproducibility with respect to bathing, dressing, bowel management, and mobility in bed [12].
Also emerging are scales that assess walking following SCI. The Walking Index for Spinal Cord Injury (WISCI), published in 2000 [13] and more recently in revised Form [14], represents an international effort to produce a complex, valid, and Spine Classifications and Severity Measures reliable tool for assessing walking independent of burden of care. Other walking tests include the Timed Up and Go (TUG), the 10 Meter Walk test, and the 6 Minute Walk Test, all three of which were recently compared on the same cohort of patients and all were found to be valid and reliable [15].
3 Summary
Where do we go from here? As summarized in a recent consensus paper generated by a working group of the ICCP (International Campaign for Cures of spinal cord injury Paralysis), the ASIA impairment scale remains the gold standard to assess neurological recovery after SCI [16]. However, this scale fails to accurately assess the thoracic spinal cord and does not include measures of pain or autonomic function, including bowel or bladder control. In addition, it is increasingly recognized that the AIS does not assess hand function with sufficient precision to distinguish subtle, but potentially important, recovery of function. The development of measures to assess these areas is of paramount importance. Moreover, the development of advanced imaging assessments including diffusion tensor magnetic resonance imaging and novel electrophysiological approaches represent areas of opportunity.
4 References
1. Lucas JT, Ducker TB (1979) Motor classification of spinal cord injuries with mobility, morbidity and recovery indices. Am Surg; 45:151–158. 2. Frankel HL, Hancock DO, Hyslop G, et al (1969) The value of postural reduction in the initial management of closed injuries of the spine with paraplegia and tetraplegia. I. Paraplegia; 7:179–192. 3. Tator CH (2006) Review of treatment trials in human spinal cord injury: issues, difficulties, and recommendations. Neurosurgery; 59:957–982. 4. Bracken MB, Collins WF, Freeman DF, et al (1984) Efficacy of methylprednisolone in acute spinal cord injury. Jama; 251:45–52. 5. Cohen M, Herbison G (1996) Content validity and reliability of the international standards for neurological classification of spinal cord injury. Top Spinal Cord Inj Rehabil; 1:15–31. 6. Marino RJ, Barros T, Biering-Sorensen F, et al (2003) International standards for neurological classification of spinal cord injury. J Spinal Cord Med; 26 Suppl 1:S50–56. 7. Coleman WP, Geisler FH (2004) Injury severity as primary predictor of outcome in acute spinal cord injury: retrospective results from a large multicenter clinical trial. Spine J; 4:373–378. 8. Geisler FH, Coleman WP, Grieco G, et al (2001) Measurements and recovery patterns in a multicenter study of acute spinal cord injury. Spine; 26:S68–86. 9. Geisler FH, Coleman WP, Grieco G, et al (2001) The Sygen multicenter acute spinal cord injury study. Spine; 26:S87–98. 10. Keith RA, Granger CV, Hamilton BB, et al (1987) The functional independence measure: a new tool for rehabilitation. Adv Clin Rehabil; 1: 6 –18. 11. Catz A, Itzkovich M, Agranov E, et al (2001) The spinal cord independence measure (SCIM): sensitivity to functional changes in subgroups of spinal cord lesion patients. Spinal Cord; 39:97–100. 12. Catz A, Itzkovich M, Steinberg F, et al (2001) The Catz-Itzkovich SCIM: a revised version of the Spinal Cord Independence Measure. Disabil Rehabil; 23:263–268. 13. Ditunno JF, Jr., Ditunno PL, Graziani V, et al (2000) Walking index for spinal cord injury (WISCI): an international multicenter validity and reliability study. Spinal Cord; 38:234–243. 14. Dittuno PL, Dittuno Jr JF, Jr. (2001) Walking index for spinal cord injury (WISCI II): scale revision. Spinal Cord; 39:654–656. 15. van Hedel HJ, Wirz M, Dietz V (2005) Assessing walking ability in subjects with spinal cord injury: validity and reliability of 3 walking tests. Arch Phys Med Rehabil; 86:190–196. 16. Steeves JD, Lammertse D, Curt A, et al (2007) Guidelines for the conduct of clinical trials for spinal cord injury (SCI) as developed by the ICCP panel: clinical trial outcome measures. Spinal Cord; 45:206–221.1 American Spinal Injury Association (ASIA) Score
Functional grades based on Frankel Grade
American Spinal Injury Association (1984) American Spinal Injury Association. Standards for neurological classification of spinal injury patients. American Spinal Injury Association: Chicago.
SCALE DESCRIPTION
Injury severity based on the following scale:
A—Complete—No motor or sensory function is preserved in the sacral segments S4–S5
B—Incomplete—Sensory but no motor function is preserved below the neurological level and includes the sacral segments S4 and S5
C—Incomplete—Motor function is preserved below the neurological level and muscle grade less than 3
D—Incomplete—Motor function is preserved below the neurological level and muscle grade of 3 or more
E—Normal—Motor and sensory function are normal
Interpretation:
Grades are presented in ascending order of severity.
References:
1. Burns SP, Golding DG, Rolle WA, Jr., et al (1997) Recovery of ambulation in motor-incomplete tetraplegia. Arch Phys Med Rehabil; 78:1169–1172. 2. Coleman W P, Geisler FH (2004) Injury severity as primary predictor of outcome in acute spinal cord injury: retrospective results from a large multicenter clinical trial. Spine J; 4:373–378. 3. Curt A, Rodic B, Schurch B, et al (1997) Recovery of bladder function in patients with acute spinal cord injury: significance of ASIA scores and somatosensory evoked potentials. Spinal Cord; 35:368–373. 4. Curt A, Keck ME, Dietz V (1998) Functional outcome following spinal cord injury: significance of motor-evoked potentials and ASIA scores. Arch Phys Med Rehabil; 79:81–86. 5. Waters RL, Adkins R, Yakura J, et al (1994) Prediction of ambulatory performance based on motor scores derived from standards of the American Spinal Injury Association. Arch Phys Med Rehabil; 75:756–760. 6. Sprigle S, Wootten M, Sawacha Z, et al (2003) Relationships among cushion type, backrest height, seated posture, and reach of wheelchair users with spinal cord injury. J Spinal Cord Med; 26:236–243. 7. Iseli E, Cavigelli A, Dietz V, et al (1999) Prognosis and recovery in ischaemic and traumatic spinal cord injury: clinical and electrophysiological evaluation. J Neurol Neurosurg Psychiatry; 67:567–571. 8. Ishida Y, Tominaga T (2002) Predictors of neurologic recovery in acute central cervical cord injury with only upper extremity impairment. Spine; 27:1652–1658. 9. Kirshblum SC, Memmo P, Kim N, et al (2002) Comparison of the revised 2000 American Spinal Injury Association classification standards with the 1996 guidelines. Am J Phys Med Rehabil; 81:502–505. 10. Scivoletto G, Morganti B, Molinari M (2004) Neurologic recovery of spinal cord injury patients in Italy. Arch Phys Med Rehabil; 85:485–489. 11. Marino RJ, Graves DE (2004) Metric properties of the ASIA motor score: subscales improve correlation with functional activities. Arch Phys Med Rehabil; 85:1804–1810. 12. Marino RJ, Ditunno JF, Jr., Donovan WH, et al (1999) Neurologic recovery after traumatic spinal cord injury: data from the Model Spinal Cord Injury Systems. Arch Phys Med Rehabil; 80:1391–1396. 13. Morganti B, Scivoletto G, Ditunno P, et al (2005) Walking index for spinal cord injury (WISCI): criterion validation. Spinal Cord; 43:27–33. 14. Priebe MM, Waring WP (1991) The interobserver reliability of the revised American Spinal Injury Association standards for neurological classification of spinal injury patients. Am J Phys Med Rehabil; 70:268–270. 15. Savic G, Bergstrom EM, Frankel HL, et al (2007) Inter-rater reliability of motor and sensory examinations performed according to American Spinal Injury Association standards. Spinal Cord; 45:444–451.