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The Journal of Bone and Joint Surgery 78:1308-14 (1996)
© 1996 The Journal of Bone and Joint Surgery, Inc.

The Relationship of Developmental Narrowing of the Cervical Spinal Canal to Reversible and Irreversible Injury of the Cervical Spinal Cord in Football Players. An Epidemiological Study*

JOSEPH S. TORG, M.D.{dagger}, R. JOHN NARANJA, JR., M.D.{ddagger}, PHILADELPHIA, HELENE PAVLOV, M.D.§, BRIAN J. GALINAT, M.D.§, RUSSELL WARREN, M.D.§, NEW YORK, N.Y. and ROBERT A. STINE, PH.D.¶, PHILADELPHIA, PENNSYLVANIA

Investigation performed at the Department of Orthopaedic Surgery, Hahnemann University Hospital; the Department of Orthopaedic Surgery, University of Pennsylvania, Philadelphia; and the Department of Orthopaedic Surgery and Radiology, The Hospital for Special Surgery, New York City


    Abstract
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
An evaluation of forty-five athletes who had had an episode of transient neurapraxia of the cervical spinal cord revealed a consistent finding of developmental narrowing of the cervical spinal canal. The purpose of the present epidemiological study was to determine the relationship, if any, between a developmentally narrowed cervical canal and reversible and irreversible injury of the cervical cord with use of various cohorts of football players as well as a large control group. Cohort I comprised college football players who were asymptomatic and had no known history of transient neurapraxia of the cervical cord. Cohort II consisted of professional football players who also were asymptomatic and had no known history of transient neurapraxia of the cervical cord. Cohort III was a group of high-school, college, and professional football players who had had at least one episode of transient neurapraxia of the cervical cord. Cohort IV comprised individuals who were permanently quadriplegic as a result of an injury while playing high-school or college football. Cohort V consisted of a control group of male subjects who were non-athletes and had no history of a major injury of the cervical spine, an episode of transient neurapraxia, or neurological symptoms. The mean and standard deviation of the diameter of the spinal canal, the diameter of the vertebral body, and the ratio of the diameter of the spinal canal to that of the vertebral body were determined for the third through sixth cervical levels on the radiographs for each cohort. In addition, the sensitivity, specificity, and positive predictive value of a ratio of the diameter of the spinal canal to that of the vertebral body of 0.80 or less was evaluated. The findings of the present study demonstrated that a ratio of 0.80 or less had a high sensitivity (93 per cent) for transient neurapraxia. The findings also support the concept that symptoms may result from a transient reversible deformation of the spinal cord in a developmentally narrowed osseous canal. The low positive predictive value of the ratio (0.2 per cent) however, precludes its use as a screening mechanism for determining the suitability of an athlete for participation in contact sports. Developmental narrowing of the cervical canal in a stable spine does not appear to predispose an individual to permanent catastrophic neurological injury and therefore should not preclude an athlete from participation in contact sports.


    Introduction
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Injuries of the cervical spine that occur during participation in football have been receiving increased attention. In 1973, Schneider observed that "the football fields of our nation have been a vast proving ground or laboratory for the study of the tragic neurologic sequelae of head and neck trauma in man." Since that time, a number of investigators have analyzed injuries of the cervical spine that have occurred during participation in American tackle football8-14. One entity, the syndrome of neurapraxia of the cervical spinal cord with transient quadriplegia, is associated with sensory or motor manifestations, or both. The sensory changes include burning pain, numbness, tingling, and loss of sensation. The motor changes range from weakness to complete paralysis of both the upper and the lower extremities. The episodes are transient, and complete sensory and motor recovery usually occurs in ten to fifteen minutes, although sometimes symptoms gradually resolve during a period of twenty-four to thirty-six hours14. An evaluation of athletes who had had transient neurapraxia of the cervical cord revealed a consistent finding of developmental narrowing of the cervical spinal canal, as an isolated entity or associated with congenital fusion of the vertebrae, protrusion of a disc, or instability of the cervical spine14. Instability was defined as radiographic evidence of more than 3.5 millimeters of translation in the anteroposterior direction or 11 degrees of angulation in the sagittal plane at a cervical vertebral segment (two adjacent vertebrae with the intervening disc)14,15. Those studies led to several clinically relevant concerns14. First, although the criterion for developmental narrowing is a ratio of the diameter of the spinal canal to that of the vertebral body of 0.80 or less, the sensitivity, specificity, and positive predictive value of this ratio in relation to transient neurapraxia of the cervical cord are unknown. Second, we wanted to determine if this ratio should be used to screen athletes for suitability for participation in contact sports. Third, we wanted to ascertain the importance of a ratio of 0.80 or less in an asymptomatic individual. Fourth, we wished to determine if an individual with developmental narrowing of the cervical spine who has had an episode of transient neurapraxia of the cervical cord is predisposed to an injury with permanent neurological sequelae. Finally, we wanted to find out if individuals who have had an episode of transient neurapraxia of the cervical cord should be excluded from participation in contact sports. We addressed these issues through an epidemiological study of various subsets of football players as well as a large control group.


    Materials and Methods
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Four groups of football players as well as a control group of 105 non-athletes were studied. Cohort I consisted of 227 college football players who were asymptomatic, had no known history of transient neurapraxia of the cervical spinal cord, and had been invited to the so-called Combine evaluation of the National Football League in 1992. (The Combine evaluates the medical history and performs a preliminary physical examination of college football players who are candidates for draft by the National Football League.)

Cohort II comprised ninety-seven professional football players who were asymptomatic and had no known history of transient neurapraxia of the cervical cord.

Cohort III consisted of forty-five high-school, college, and professional football players who had sustained at least one episode of transient neurapraxia of the cervical spinal cord and had been referred to the senior one of us (J. S. T.) for evaluation. Twenty-two of these athletes returned to at least their former level of competition. Seven had evidence of a herniated nucleus pulposus or a bulging disc, five had evidence of instability, three had spondylosis, and five had congenital fusion of the cervical spine. All recovered completely and were asymptomatic.

Cohort IV consisted of seventy-seven former athletes who were permanently quadriplegic as a result of a football injury in high school or college. These individuals were found from a listing of athletes in the National Football Head and Neck Injury Registry12,13. Fifty-nine (77 per cent) of the individuals in this group had sustained the injury as a result of a burst fracture, and eighteen (23 per cent) had sustained it as a result of a unilateral or bilateral facet dislocation. There were no injuries secondary to a herniated disc, and none of the individuals had normal findings on radiographs of the spine. Four individuals in the cohort were found to have an incomplete lesion of the spinal cord.

Cohort V, the control group of non-athletes, consisted of 105 male subjects who were fifteen to thirty-eight years old and had been evaluated at The Hospital for Special Surgery because of symptoms related to the neck. None of the subjects had a history of a major injury of the cervical spine, an episode of transient neurapraxia, or neurological symptoms.

The ratio of the diameter of the spinal canal to that of the vertebral body was determined on plain radiographs, according to the technique described by one of us (H. P.) and colleagues5, at the third through sixth cervical levels. The ratio is determined by measuring the distance from the mid-point of the posterior aspect of the vertebral body to the nearest point on the corresponding spinolaminar line and dividing this value by the anteroposterior diameter of the vertebral body on a lateral radiograph. The anteroposterior measurement of the vertebral body is made at the mid-portion of the vertebral body to avoid the effect of osteophytes. Variations in radiographic technique are minimized because both the spinal canal and the vertebral body are similarly affected by magnification factors regardless of target and object distances.

The mean, standard deviation, and number of observations of the sagittal diameter of the spinal canal, the sagittal diameter of the vertebral body, and the ratio of these diameters at the third through sixth cervical levels were determined for each of the five study cohorts (Table I). The means for the cohorts were compared, and one-way analysis of variance was used to detect a difference among the cohorts at each vertebral level. It is important to note that this analysis does not indicate which cohorts differ from each other; it can only demonstrate that a difference exists. Subsequently, to obtain pairwise comparisons, the method of Tukey and Kramer2 was applied. This method also allowed for unequal sizes of cohorts.


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TABLE I MEASUREMENTS OF THE SPINAL CANAL AND VERTEBRAL BODIES AND THE RATIOS OF THESE MEASUREMENTS

 
We then determined the sensitivity, specificity, and positive predictive value of the threshold of 0.80 for the ratio of the diameter of the spinal canal to that of the vertebral body for the presence of developmental narrowing. Sensitivity is the probability of obtaining a positive result in an individual who has the disease—that is, the probability of obtaining a ratio of 0.80 or less in an individual who has symptoms of neurapraxia of the cervical spinal cord. Specificity is the probability of obtaining a negative result in an individual who does not have the disease—that is, the probability of obtaining a ratio of more than 0.80 in an asymptomatic individual. The positive predictive value defines the likelihood that a patient who has a positive finding actually has the disease. In the present report, the positive predictive value is the percentage of individuals who had symptoms in the group that had a ratio of 0.80 or less. For the purposes of this calculation, the rate at which neurapraxia of the cervical spinal cord has been found to occur in football players at the intercollegiate level (7.3 per 10,000 athletes) was obtained from data in a previous study14.

In order to determine whether transient neurapraxia of the cervical spinal cord is associated with an increased risk of permanent quadriplegia, a mail and telephone survey of the seventy-seven former athletes who had permanent quadriplegia (Cohort IV) was conducted. The survey was performed by one research associate, who used a questionnaire to ascertain whether those individuals had had neurological symptoms in the recent or distant past before the catastrophic injury. Also, a follow-up examination of the forty-five patients who had had an episode of transient neurapraxia of the cervical spinal cord (Cohort III) was performed in order to determine if any of the patients had subsequently sustained a permanent neurological injury.


    Results
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Plotting the distribution of the ratios demonstrated a normal distribution curve for each cohort. One-way analysis of variance identified a difference among the cohorts with regard to the mean diameter of the spinal canal, the mean diameter of the vertebral body, and the mean ratio of these diameters (Figs. 1, 2, and 3). Post hoc comparisons of pairs with use of the method of Tukey and Kramer2 revealed that the mean diameter of the cervical spinal canal and the mean ratio in Cohort III were significantly smaller than those in the other four cohorts (p < 0.05). With the numbers available, the paired analysis revealed no difference among the mean diameters of the cervical spinal canal of the other cohorts. An analysis of the ratios only demonstrated paired differences between Cohort I and Cohort V (p < 0.001) and between Cohort II and Cohort V (p < 0.001). There was no difference in the ratios between Cohort IV and Cohort V. Cohort IV also had a significantly larger mean ratio than Cohorts I, II, and III (p < 0.001) (Table I).



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Profile plot of the mean diameters of the spinal canal, demonstrating a significantly smaller value in Cohort III compared with that in all of the other cohorts (p < 0.05). With the numbers available, no significant difference was found among Cohorts I, II, IV, or V.

 


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Profile plot of the mean diameters of the vertebral bodies, demonstrating a significantly smaller value in Cohort V compared with that in all of the other cohorts (p < 0.05). The diameter in Cohort IV was found to be significantly smaller than that in Cohorts I, II, and III (p < 0.05) but larger than that in Cohort V.

 


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Profile plot of the ratio of the diameter of the spinal canal to that of the vertebral body, demonstrating a significantly smaller ratio in Cohort III compared with that in all of the other cohorts (p < 0.05). In addition, Cohort V had a significantly higher mean ratio than that for Cohorts I, II, and IV (p < 0.05). However, this result must be interpreted in light of the larger vertebral bodies in the latter three cohorts.

 
No apparent relationship was found between the ratio of the spinal canal to that of the vertebral body and the incomplete lesions in Cohort IV. Two of the four quadriplegic individuals who had an incomplete lesion had a ratio of 0.80 or less, and two had a ratio that was more than 0.80.

Calculations for sensitivity revealed that forty-two of the forty-five athletes who had transient neurapraxia of the spinal cord (Cohort III) had a ratio of 0.80 or less at one level or more; thus, the sensitivity was 93 per cent (95 per cent confidence interval, 82 to 97 per cent).

Ninety-three (41 per cent) of the 227 asymptomatic college football players (Cohort I) had a ratio of 0.80 or less at one level or more. Thus, the specificity for this cohort was 59 per cent (95 per cent confidence interval, 53 to 64 per cent). Forty-one (42 per cent) of the ninety-seven asymptomatic professional players (Cohort II) had a ratio of 0.80 or less at one level or more. Thus, the specificity for this cohort was 58 per cent (95 per cent confidence interval, 48 to 67 per cent).

None of the seventy-seven quadriplegic individuals (Cohort IV) who were contacted by telephone or mail reported an episode of transient quadriplegia before the major injury. Also, none of the forty-five athletes who had symptoms of transient neurapraxia of the cervical cord (Cohort III) had a subsequent injury that resulted in a permanent neurological deficit.


    Discussion
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Since 1986, when transient neurapraxia of the cervical cord was first described14, a number of issues concerning the disorder have arisen. The purpose of the present epidemiological study was to address those issues, which include the relationship of developmental narrowing of the cervical spinal canal to reversible and irreversible injury of the cervical cord.

The data in the present study indicate that, with a few exceptions, individuals who have had an episode of transient neurapraxia of the cervical cord that included sensory or motor symptoms, or both, have a spinal canal and vertebral body ratio of 0.80 or less at one level of the cervical spine or more. The importance of the determination of this ratio on radiographs, in addition to avoiding magnification error, has been the demonstration of the pathophysiological basis for transient neurapraxia of the cervical cord14—that is, the developmental narrowing of the spinal canal in the anteroposterior plane that is associated with extreme flexion or extension of the spine can result in transient compression of the cord. This has been described previously by Penning as the pincer mechanism. Specifically, when the cervical spine is in hyperextension, the posteroinferior aspect of the superior vertebral body and the anterosuperior aspect of the lamina of the subjacent vertebra approximate and, conversely, when the cervical spine is in flexion, the lamina of the superior vertebra and the posterosuperior aspect of the subjacent vertebral body approximate, causing a sudden decrease in the anteroposterior diameter of the canal at that point and resulting in compression of the spinal cord. On the basis of a review of the records of seventy-seven athletes (the forty-five athletes in Cohort III and thirty-two athletes reported on in a previous study14) who had symptomatic developmental narrowing of the cervical cord that was uncomplicated by instability or herniation of a disc, it was concluded that the neurological manifestations of transient neurapraxia of the cervical cord are temporary and completely reversible14.

The low specificity of the ratio in Cohorts I, II, and IV appeared to be due to anthropometric differences. There may be a natural selection process in which an individual who has a particular body type (for example, mesomorphic) is better suited for playing competitive football. Specifically, the physical characteristics of the cervical spine in the individuals in Cohorts I and II included relatively larger vertebral bodies than those of the other cohorts, but the mean diameters of the canal were similar to those of the other cohorts except those of Cohort III. Other investigators1,3,4 have confirmed this finding. Therefore, determinations of the ratio in those individuals must be interpreted with caution. The asymptomatic individuals in Cohorts I and II may have had a ratio of 0.80 or less at one level or more without true narrowing of the cervical spinal canal—that is, the diameter of the cervical spinal canal might have been adequate despite the large diameters of the vertebral bodies. Nevertheless, the ratio remains an important tool for identifying a narrowed canal. It is important to remember, however, that the ratio is sensitive but not specific.

In a previous report14, neurapraxia of the cervical spinal cord was found to occur at a rate of 7.3 per 10,000 in athletes who played intercollegiate football. In the present study, ninety-three (41 per cent) of 227 college football players who had no symptoms and no history of transient neurapraxia of the cervical cord had a ratio of the diameter of the spinal cord to that of the vertebral body of 0.80 or less. Therefore, it could be extrapolated that 41 per cent (4100) of 10,000 participants would have a ratio of 0.80 or less at one cervical level or more. If it is assumed that all symptomatic athletes who play football at the intercollegiate level have a ratio of 0.80 or less, then the positive predictive value for the development of transient neurapraxia of the cervical cord in such an individual is 7.3 per 4100 (0.2 per cent). A positive predictive value of 0.2 per cent indicates that the ratio should not be used to determine suitability for participation in contact sports.

Of the forty-five high-school, college, and professional football players who had had at least one episode of transient neurapraxia of the cervical cord (Cohort III), forty-two (93 per cent) had developmental narrowing of the cervical spinal canal as determined by a ratio of 0.80 or less at one level or more. The mean anteroposterior diameter of the spinal canal in Cohort III and Cohort IV was 15.3 millimeters and 18.9 millimeters, respectively. Thus, Cohort III was significantly different from Cohort IV with respect to both the ratio and the actual diameter of the spinal canal (p < 0.05). Also, the mean anteroposterior diameter of the spinal canal in Cohort IV was essentially identical to the diameter in Cohorts I, II, and V. A smaller mean anteroposterior diameter would be an expected finding if developmental narrowing of the spinal canal played an important role in the etiology of neurapraxia and was associated with permanent neurological loss. In addition, the anteroposterior dimensions of the vertebral bodies in Cohort IV were significantly smaller than those in Cohorts I, II, and III (p < 0.05). This may indicate that permanent neurological loss results from an injury of a vertebral body that is radiographically smaller and that fails during axial loading. Axial load8,10-13, the degree of instability8,11, and the duration from the injury to the reduction8,12 have been implicated as factors in the occurrence of permanent neurological injury in athletes who play tackle football. Moreover, none of the seventy-seven quadriplegic individuals (Cohort IV) in our study had had an episode of neurapraxia of the spinal cord before the catastrophic injury. Also, none of the forty-five high-school, college, and professional players who had had an episode of transient neurapraxia (Cohort III) became quadriplegic. These data, in combination with the absence of developmental narrowing of the cervical canal in Cohort IV, provide evidence that the occurrence of transient neurapraxia of the cervical cord and an injury associated with permanent catastrophic neurological sequelae are unrelated. Therefore, developmental narrowing of the cervical cord in a spine that has no evidence of instability is neither a harbinger of nor a predisposing factor for permanent neurological injury. Our data did not reveal an association between developmental narrowing of the cervical canal and quadriplegia. We believe that the major factor in the occurrence of cervical quadriplegia in football players is a tackling technique in which the head is used as the primary point of contact, with resulting transmission of axial energy to, and subsequent failure of, the cervical spine8,10-13. (It is of note that discovery of the relationship between axial loading and cervical quadriplegia in football players led to the prohibition of spearing and head-impact techniques in high-school and college football. The prohibition has resulted in a marked decrease in the prevalence of permanent cervical quadriplegia in athletes9,10,13.) In addition, the random distribution of the ratios for the quadriplegic individuals (Cohort IV) may explain the coexistence of a developmentally narrowed cervical canal and quadriplegia.

The findings of the present study demonstrated the high sensitivity, low specificity, and low positive predictive value of the ratio of the diameter of the cervical spinal canal to that of the vertebral body, precluding its use as a screening mechanism for determining the suitability of an individual for participation in contact sports. We believe that developmental narrowing of the cervical canal without associated instability does not predispose an individual to permanent catastrophic neurological injury and, therefore, should not preclude an athlete from participation in contact sports.


    Footnotes
 
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.

{dagger}Hahnemann University Hospital, Broad and Vine Streets, Mail Stop 989, Philadelphia, Pennsylvania 19102.

{ddagger}Department of Orthopaedic Surgery, University of Pennsylvania School of Medicine, 3400 Spruce Street, Philadelphia, Pennsylvania 19104.

§The Hospital for Special Surgery, 535 East 70th Street, New York, N.Y. 10021.

¶Department of Statistics, The Wharton School of the University of Pennsylvania, 3000 Steinberg Hall-Dietrich Hall, Philadelphia, Pennsylvania 19104-6302.


    References
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Herzog, R. J.; Wiens, J. J.; Dillingham, M. F.; and |and |Sontag, M. J.: Normal cervical spine morphometry and cervical spinal stenosis in asymptomatic professional football players: plain film radiography, multiplanar computed tomography, and magnetic resonance imaging. Spine, 16(6S): 178-S186, 1991.

  2. Kirk, R. E.: Experimental Design: Procedures for the Behavioral Sciences, section 3.5. Belmont, California, Brooks/Cole, 1982.

  3. Matsuura, P.; Waters, R. L.; Adkins, R. H.; Rothman, S.; Curbani, N.; and |and |Sie, I.: Comparison of computerized tomography parameters of the cervical spine in normal control subjects and spinal cord-injured patients. J. Bone and Joint Surg., 71-A: 183-188, Feb. 1989.[Abstract/Free Full Text]

  4. Odor, J. M.; Watkins, R. G.; Dillin, W. H.; Dennis, S.; and |and |Saberi, M.: Incidence of cervical spinal stenosis in professional and rookie football players. Am. J. Sports Med., 18: 507-509, 1990.[Abstract/Free Full Text]

  5. Pavlov, H.; Torg, J. S.; Robie, B.; and |and |Jahre, C.: Cervical spinal stenosis: determination with vertebral body ratio method. Radiology, 164: 771-775, 1987.[Abstract/Free Full Text]

  6. Penning, L.: Some aspects of plain radiography of the cervical spine in chronic myelopathy. Neurology, 12: 513-519, 1962.

  7. Schneider, R. C.: Head and Neck Injuries in Football. Mechanisms, Treatment, and Prevention. Baltimore, Williams and Wilkins, 1973.

  8. Torg, J. S.; Sennett, B.; Vegso, J. J.; and |and |Pavlov, H.: Axial loading injuries to the middle cervical spine segment: an analysis and classification of twenty-five cases. Am. J. Sports Med., 19: 6-20, 1991.[Abstract/Free Full Text]

  9. Torg, J. S.; Vegso, J. J.; O'Neill, M. J.; and |and |Sennett, B.: The epidemiologic, pathologic, biomechanical, and cinematographic analysis of football-induced cervical spine trauma. Am. J. Sports Med., 18: 50-57, 1990.[Abstract/Free Full Text]

  10. Torg, J. S.; Vegso, J. J.; Sennett, B.; and |and |Das, M.: The National Football Head and Neck Injury Registry: 14-year report on cervical quadriplegia, 1971 through 1984. J. Am. Med. Assn., 254: 3439-3443, 1985.[Abstract/Free Full Text]

  11. Torg, J. S.; Pavlov, H.; O'Neill, M. J.; Nichols, C. E., III; and |and |Sennett, B.: The axial load teardrop fracture: a biomechanical, clinical, and roentgenographic analysis. Am. J. Sports Med., 19: 355-364, 1991.[Abstract/Free Full Text]

  12. Torg, J. S.; Truex, R. C., Jr.; Marshall, J.; Hodgson, V. R.; and |and |Quedenfeld, T. C.: Spinal injury at the level of the third and fourth cervical vertebrae from football. J. Bone and Joint Surg., 59-A: 1015-1019, Dec. 1977.[Abstract/Free Full Text]

  13. Torg, J. S.; Truex, R., Jr.; Quedenfeld, T. C.; Burstein, A.; Spealman, A.; and |and |Nichols, C., III: The National Football Head and Neck Injury Registry. Report and conclusions. J. Am. Med. Assn., 241: 1477-1479, 1979.[Abstract/Free Full Text]

  14. Torg, J. S.; Pavlov, H.; Genuario, S. E.; Sennett, B.; Wisneski, R. J.; Robie, B. H.; and |and |Jahre, C.: Neurapraxia of the cervical spinal cord with transient quadriplegia. J. Bone and Joint Surg., 68-A: 1354-1370, Dec. 1986.[Abstract/Free Full Text]

  15. White, A. A., III; Johnson, R. M.; Panjabi, M. M.; and |and |Southwick, W. O.: Biomechanical analysis of clinical stability in the cervical spine. Clin. Orthop., 109: 85-96, 1975.


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