|William B. Barr, PhD, ABPP|
Associate Professor of Neurology & Psychiatry,
NYU School of Medicine
This year marks the 20th anniversary of the “modern era” in the study of concussion in sports, which began in 1994 following the retirements of Merrill Hoge and Al Toon and the National Football League’s (NFL) formation of its first Mild Traumatic Brain Injury Committee. Since that time, we have witnessed a marked shift from what was a pervasive attitude of denying or minimizing the effects of head injury in sport to one where stories of the current “concussion epidemic” or the controversy about long-term consequences of head injury in retired athletes appear in our newspapers on a daily basis. Over the same time period, the field of neuropsychology has received an unprecedented degree of public attention resulting from the fact that many in our field, including members of the Society of Clinical Neuropsychology (SCN), have provided important contributions to the scientific study of sports concussion and development of methods for its assessment. My goal in this SCN NeuroBlog is to provide a brief review and critique of neuropsychology’s role in the clinical management of sports concussion with suggestions on how we can maintain our position as leaders with regard to this highly publicized injury.
At the beginning of concussion’s modern era, it was not uncommon to hear statements from other health professionals that we were in the infancy in the study of the head injury and without any available scientific information to guide clinical management. Any practicing neuropsychologist at that time knew that this was not the case. We were well aware that Dorothy Gronwall and her colleagues in New Zealand had published a number of groundbreaking studies during the 1970’s, using neuropsychological methods for tracking information-processing capacity following minor head injury. During the 1980’s, Jeffrey Barth, Sureyya Dikmen, and Harvey Levin and colleagues had all conducted a number of important investigations in the United States using neuropsychological test batteries to characterize outcomes in mild head injured subjects. The results of those studies demonstrated that recovery from milder forms of head injury was characterized by a complex interaction of cognitive, somatic, and emotional factors with the expression of symptoms influenced significantly by a range of psychosocial factors.
Armed with the findings from studies listed above, clinical neuropsychologists were well prepared in the 1980’s and 1990’s to conduct a comprehensive assessment of symptoms in patients they encountered following what was eventually termed as mild traumatic brain injury (MTBI). Many at that time continued to use the Halstead-Reitan Neuropsychological Test Battery for evaluation of these patients. However, an increasing number of practitioners began to use a more flexible approach to neuropsychological assessment, with test batteries comprised of measures of intelligence, attention, executive functions, and memory. It is important to note that, most clinicians were also including measures of symptom reporting in their test batteries, using standardized measures such as the Minnesota Multiphasic Personality Inventory (MMPI) and its descendants. While the clinical batteries often took numerous (3-6) hours to complete, they provided the most effective means known at that time for evaluating symptoms in patients with MTBI.
Neuropsychology’s approach to head injury received a substantial boost in the late 1980’s following research performed by Barth, Macciocchi and colleagues at the University of Virginia, who developed the methodology for obtaining empirical data on concussion through controlled prospective studies of athletes following head injury. Their model of data collection, now known as the Sports Laboratory Assessment Model (SLAM) consisted of obtaining preseason neuropsychological test data to serve as a baseline in athletes at risk for sustaining a concussion during competition and repeating the same tests in injured athletes and matched controls on a serial basis to measure the effects of the injury and its pattern of recovery. Among the major findings from early studies using the SLAM methodology were that neuropsychological tests were established as being sensitive to the effects of concussion and that those effects were observed to clear rather rapidly, within a period of 5 to 10 days, in the vast majority of cases.
Given the fact that results from standard imaging and electrophysiological studies were usually negative in athletes following concussion, the hope in the beginning of the modern era of sports concussion management was that neuropsychological testing would provide most effective means for assessing symptoms during recovery. The SLAM methodology was promptly adapted for clinical use by a number of neuropsychologists working primarily with collegiate and professional football teams. Brief test batteries were assembled and administered to entire teams through large-scale baseline testing programs. The length of the test batteries was kept to less than 30 minutes, understanding the need to limit the time burden for the athletes and the assessment team. The test batteries were limited in contents to measures of attention, processing speed, and memory, while also including a brief measure of post-concussion symptoms. The belief was that, due to athletes’ reputed tendency to minimize symptoms, information from the neurocognitive tests administered serially following injury would provide the most accurate means for tracking the effects of the injury and marking the time course of its recovery.
The baseline testing programs in sports began with the use of paper-pencil tests that were readily available to all licensed neuropsychologists. However, those tests were soon replaced by computerized test batteries developed specifically for assessment of concussion symptoms in athletes, which were promoted and sold via a large-scale marketing campaign to physicians, certified athletic trainers, and other clinicians in addition to neuropsychologists. The computerized tests were claimed by their developers to provide an advantage over the paper-pencil tests by providing a more sensitive, reliable, and efficient means of assessing concussion symptoms. Through substantial media exposure, the brand names of computerized tests became synonymous with baseline testing in sports, with the science and methodology of clinical neuropsychology relegated to a less prominent role.
While sportscasters, the media, and the public at large were emphasizing the use of baseline testing in sports, there was a controversy developing within the field of neuropsychology regarding its ultimate benefits. Some investigators began to question the increasing use of this methodology, given the lack of empirical support, particularly from investigative teams that were independent of the test developers. This was followed by studies, emerging over time, demonstrating that information from neuropsychological tests added little to the assessment of acute post-concussion symptoms compared to what was obtained through a more brief form of sideline testing using a combination of symptom questionnaires, balance measures, and a brief screen of cognitive functioning.
Results from other investigations began to show that many of the tests used for serial testing in athletes demonstrated unacceptably low levels oftest-retest reliability in addition to disappointing levels of sensitivity/specificity for detecting the effects of concussion. The validity of the baseline test performance came into question when measures were administered on a group basis, as suggested by the manufacturers. Athletes began to realize the benefits of underperforming on baseline testing so that the effects of concussion would be obscured on repeat testing following injury, affecting the validity of a growing number of baseline assessments. Further complications began to emerge from the fact that practitioners without adequate training in psychometrics and brain-behavior relations were often the ones obtaining the test results following injury, causing them in many cases to make serious interpretive errors. Based on these findings and trends, an international panel of experts on concussion in sports concluded in statements published in 2012 that, “there is insufficient evidence to recommend the widespread routine use of baseline neuropsychological testing.”
Turning to what we have learned over the past 20 years, there has been a convergence of information obtained through studies of animal models and humans indicating that the acute physiological effects and symptoms associated with concussion resolve within 7-10 days in the vast majority (80%-95%) of injured athletes, upholding the findings originally reported much earlier by University of Virginia group. While cognitive deficits are known to be present during the acute time period, neuropsychological testing does not appear to be the optimal choice for assessment at that time, since symptoms can be monitored effectively through briefer sideline test procedures using the Sports Concussion Assessment Tool (SCAT-3).
However, as most neuropsychologists know, there are those individuals, including athletes, who continue to report symptoms well beyond the window of typical recovery from concussion. These individuals, exhibiting symptoms of what we term as post-concussion syndrome (PCS), create clinical conundrums for most clinicians involved in concussion management. I argue that this is the group on whom neuropsychologists should be focusing attention. As a result of neuropsychologists’ unique combination of training and use of empirically advanced assessment techniques, we are the group of professionals who can provide the most valuable input for diagnosis and management for of individuals with PCS.
Investigators focusing on the search for the elusive biomarker of concussion often ignore the fact that the diagnosis of concussion and subsequent PCS is based primarily on a subject’s subjective account of his or her symptoms. We are well aware that the reporting of those symptoms can be affected substantially by a number of “non-injury” factors. To begin with, research has shown that those with PCS commonly experience co-morbid conditions such as mood disorder, chronic pain, attention deficit hyperactivity disorder (ADHD), or the effects of somatization, all of which can result symptoms overlapping with those commonly reported in PCS. We are also aware that a number of “normal” psychological factors secondary to misattribution of symptoms, including “expectation as etiology”, the “diagnosis threat”, and the “good old days” phenomenon can influence symptom expression in that group. We are likely to be seeing an increase in the frequency of these misattribution phenomena as a result of increased availability of information related to concussion available through the popular media and Internet. Using our strengths in clinical assessment, neuropsychologists are in an excellent position to serve as those members of the treatment team who are in the best position to identify and treat the co-morbid conditions and other important “non-injury” factors that can influence the reporting of PCS symptoms in athletes and other groups.
My belief is that the optimal time for a referral to clinical neuropsychologists in a sports concussion setting is not immediately following the injury, but when the athlete is continuing to report symptoms for a period of 14-days or more. At that relatively early time point, he or she will have passed through the typical period of symptom recovery but will have not yet reached the critical juncture when PCS symptoms have become chronic and possibly intractable in nature. A comprehensive neuropsychological evaluation using tests of cognitive functioning, self-report, and performance validity performed at that time will provide the clinician with valuable diagnostic data and information to guide recommendations for subsequent intervention. As demonstrated in clinical studies, early identification and treatment of the co-morbid conditions and psychological factors provides the most effective means known for preventing the development of long-term PCS symptoms.
In conclusion, while we can admire our field’s initial attempt to offer neuropsychological testing as the primary tool for tracking the acute symptoms of concussion in athletes, it is time to admit that these watered-down test batteries did not end up being as useful as we had hoped. My opinion is that clinical neuropsychologists can now play a more important and useful role in the management of sports concussion by going back to where we were 20 years ago by providing evaluations of athletes using more comprehensive test batteries prior to development of chronic PCS symptoms. I am not suggesting that we return to the use of 3-6 hour test batteries with all of these athletes. We can clearly benefit from advances in test development and clinical studies of concussion to narrow our test batteries down to less than two hours, including the use of a comprehensive symptom measure such as the MMPI-2-RF. In the end, returning to the “psychology” in neuropsychology will enable us to provide a unique perspective to the modern treatment team that has evolved for assessment and treatment of sports concussion and help many of our athletes obtain the services they need to reach a full and successful recovery.