Clinical Studies
Immediate Neurocognitive Effects of Concussion

DISCUSSION

Definition of concussion

Although it is still commonly assumed that LOC is a defining and essential feature of concussion, research and clinical experience in the neurosciences have indicated for more than 30 years that an individual can experience concussion without LOC (14). C.M. Fisher noted in 1966 that confusion and amnesia are the hallmarks of concussion (15). Results from this prospective study on the immediate effects of concussion now demonstrate that significant neurocognitive changes can be detected after injury without LOC, PTA, or physical neurological abnormalities. Nearly 85% of the injured subjects in this study experienced no LOC, PTA, or change in gross neurological status but exhibited measurable deficits in orientation, concentration, and memory function in standardized mental status testing immediately after concussion.

All injured subjects in this study sustained concussion according to standard definitions accepted by the American Academy of Neurology (3) and the American Congress of Rehabilitation Medicine (4). Subjects who experienced "ding" injuries (concussion without LOC or PTA) exhibited significant deterioration from their preinjury baseline levels of cognitive functioning. These findings are consistent with earlier research suggesting that neurocognitive functioning is the component of neurological status that is most susceptible to change after MTBI (30), thus indicating the need for detailed mental status testing to detect subtle abnormalities, even in cases without documented LOC or PTA. As indicated by the current findings, sensitive testing of orientation, concentration, and memory is critical for assessment of subtle mental status changes after concussion.

Severity of injury

The severity of neurocognitive abnormalities detected in standardized testing immediately after injury in this study was correlated with established indicators of injury severity (i.e., LOC and PTA) (23). Subjects who experienced a brief period of PTA after injury were immediately more impaired than those who did not experience PTA, and subjects who sustained observed LOC displayed the most severe neurocognitive impairment immediately after concussion. Empirical evidence from this prospective study of human subjects supports results from earlier animal research models (33) of MTBI, suggesting that concussive brain injury may occur in the absence of LOC but that more severe grades of cerebral trauma are manifest in more observable neurological dysfunction and neurocognitive impairment. These findings indicate that MTBIs without LOC or PTA are associated with measurable neurocognitive deficits (as assessed with objective testing)that have not been previously appreciated, and they provide perhaps the first clinical evidence of a minimal threshold for the effects of concussion on brain function among human subjects.

With respect to sports-related head injuries, PTA and LOC have been emphasized differently by the Colorado Medical Society (13), Cantu (9), and American Academy of Neurology (3) grading scales for concussion severity, on the basis of the clinical experience of experts in the absence of prospective scientific data (Table 5). These data are the first to demonstrate that PTA and LOC are manifestations of increasing concussion severity, consistent with the grading scale outlined in the Colorado Medical Society Guidelines for the Management of Concussion in Sports (13, 21). When neurocognitive deficits are measured at the time of concussion, it becomes apparent that PTA and LOC reflect a severity gradient of traumatic pathophysiological processes that adversely affect brain function.

Patterns of recovery

TABLE 4. Standardized Assessment of Concussion Scores for Injured Subjects, with or without Loss of Consciousness or Posttraumatic Amnesia, at Preseason Baseline Times, the Time of Injury, and 15 min, 48 h, and 90 d after Injury^a

^aSAC, Standardized Assessment of Concussion; LOC, loss of consciousness; PTA, posttraumatic amnesia. Values are mean + standard deviation.

Significant group differences: total score [ F(2,88) = 53.08, P < 0.0001], orientation [ F(2,88) = 19.07, P < 0.0001], immediate memory [ F(2,88) = 31.73, P < 0.0001], concentration [ F(2,88) = 5.39, P < 0.006], delayed recall [ F(2,88) = 18.47, P < 0.0001]. The LOC group was significantly below the no LOC/no PTA group in the SAC total score and all subtest scores. The PTA group was significantly below the no LOC/no PTA group in the SAC total, immediate memory, and delayed recall scores. The LOC group was significantly below the PTA group in immediate memory score.

FIGURE 3. Mean SAC total scores at preseason baseline, the time of injury, and 15 minutes, 48 hours, and 90 days after injury for subjects with or without LOC or PTA.

TABLE 5. Diagnostic Grading Scales for Sports-related Concussion

Our findings are also informative with respect to the early natural history of neurocognitive abnormalities during the acute phase of MTBI. The empirical data on the immediate effects of MTBI collected in this study reflect the subjective experience described by many MTBI patients, with a course characterized by more severe disruption of cognitive functioning immediately after injury, followed by gradual recovery within several hours and full recovery to baseline cognitive and functional status within a few days. This study provides the first large data set demonstrating the slope of the neurocognitive recovery curve early after MTBI. Injured subjects without PTA or LOC displayed the fastest recovery during the acute phase, without significant cognitive impairment(as a group) by 15 minutes after injury. Interestingly, subjects who experienced sustained LOC remained more impaired than did subjects without LOC or PTA at 15 minutes but closed the gap of recovery within 2 days, such that there were no statistically significant differences between the three clinical groups at 48 hours after injury. Nearly all subjects, with or without LOC and PTA, demonstrated full recovery with the SAC within 2 days after injury.

Although these findings may be interpreted as indicating that LOC and PTA do not predict short-term (i.e., 48-h) recovery after concussion, caution must be exercised. The sample of subjects who sustained either LOC or PTA was relatively small, and the durations of LOC and PTA in this study were quite short. The range of injury severity in this study was also quite limited, i.e., only relatively mild forms of TBI, with no grave neurological sequelae or permanent residual impairment. Additionally, assessment of "recovery" in this study was based solely on a brief neurocognitive screening measure and did not include more extensive neuropsychological testing, neurological examinations, or advanced neuroimaging studies. We were not able to clarify the effects of recurrent concussion, because none of our injured subjects sustained more than one injury. This study did not include normal control subjects in the true sense, but a recent report (5) on noninjured control subjects who were retested at the same intervals as injured subjects supports the main findings of our study. Additional studies are underway to correlate data from brief mental status screening measures with more extensive neuropsychological testing results and to address the issue of practice effects on serial cognitive testing and the associated effects on interpretation of cognitive recovery after concussion.

Study limitations and future considerations

The infrequent occurrence of LOC and PTA limits our interpretation of the rate and trajectory of recovery by the three clinical groups and highlights the need for very large multisite research initiatives to accrue enough head injuries of varying severity for study. The design of this study unfortunately does not provide more detailed data on the dynamics of cognitive recovery by subjects with PTA and LOC between 15 minutes and 48 hours after injury. Our findings demonstrate the need for further study of recovery during the first 24 hours after concussion. Initial injury severity did not systematically affect subject attrition rates at the various postinjury assessment points (i.e., with more severely injured subjects being more likely to undergo reassessment), but practical factors (e.g., athletic trainer clinical demands during games) complicate the collection of acute injury data even in a sports-related head injury research model.

More empirical data on the immediate and long-term effects of sports-related concussion are needed to establish the relative importance of PTA, LOC, and other factors for the classification of injury severity, the implementation of concussion management strategies, and the development of evidence-based return-to-play guidelines (12). This study makes clear, however, the importance of systematic assessment of cognitive functioning at the time of concussion for accurate grading of injury severity. A delay of even 24 hours before formal assessment of the neurocognitive status of injured subjects significantly limits the accuracy of injury severity classifications and predictions of the expected course of postconcussion recovery.

CONCLUSION

Clinicians responsible for the care of injured athletes should be aware that sports-related concussion most often occurs in the absence of observed LOC or classic PTA and that the presence of LOC or PTA indicates a more severe grade of injury during the acute phase. In all cases of head injury, with or without PTA or LOC, the player’s postinjury recovery should be closely monitored for several days. All relevant clinical information must be considered in decision-making regarding a player’s readiness to return to play after concussion.

This report is the first to prospectively measure the immediate neurocognitive effects of concussion, correlate the severity of neurocognitive impairment with the occurrence of LOC and PTA, and illustrate the early course of postinjury recovery. Our findings indicate the need for systematic assessment of neurocognitive functioning during the acute phase, in addition to conventional inquiries regarding the occurrence of LOC and PTA, for classification of injury severity. Beyond the context of sports-related head injuries, improved methods of acute concussion assessment may be helpful in identifying patients evaluated in other trauma settings (e.g., hospital emergency departments) who are potentially at risk for more severe neurosurgical complications or persistent symptoms after TBI.

ACKNOWLEDGMENTS

We thank all of the certified athletic trainers who were instrumental in data collection as part of this study. We also acknowledge the players, coaching staff, and administration of each participating institution for their cooperation throughout this study.

Received, August 3, 2001.
Accepted, December 14, 2001.
Reprint requests: Michael McCrea, Ph.D., Neuropsychology Service, Waukesha Memorial Hospital, 721 American Avenue, Suite 501, Waukesha, WI 53188.
Email: michael.mccrea@phci.org

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