In 2009 investigators Dr. Ben Omalu and, subsequently, Dr. Ann McKee, released landmark studies on the brains of retired NFL players and other high impact athletes. They documented a rare neuro-pathological/neurodegenerative disorder known as chronic traumatic encephalopathy (CTE). Since that study researchers have begun to look at the long term effects of concussion and sub-concussive hits on retired NFL alumni. One such study commissioned by the NFL found that 6.1 percent of all players over the age of 50 were likely to receive a diagnosis of dementia, AD, or other form of dementia (which is over five times what is expected in those of similar age in the general population). More shocking were the numbers on the 50 and under age group, who were 20 times more likely to carry one of the aforementioned diagnosis when compared to age matched non-alumni.7 Overall, retired NFL players are three times more likely to die of a neurodegenerative disorder and four times more likely to die of AD or ALS.7
CONCUSSION EVALUATION AND MANAGEMENT
The National Football League (NFL) now has the most comprehensive concussion management program of any professional sports league. The program is administered by the Head, Neck and Spine Medical Committee, which is chaired by two neurosurgeons and recenlty incorporated a neurologist. As a result of the collective bargaining agreement, any recommendations from the committee must be cleared by the NFL Players Association (NFL-PA) Mackey-White concussion committee, which currently has four member neurologists.
Players are required to undergo a preseason comprehensive neurological evaluation that includes concussion history and baseline evaluation, i.e. a tablet based NFL sideline concussion tool along with computerized neuropsychological testing (most teams use IMPACT). Additionally, all team locker rooms have an educational poster about sports concussion. 8
In 2012 the NFL enacted a new rule that during each game a non-affiliated athletic trainer be situated in the press box to monitor the field and sidelines for potential concussions. If a concussion is suspected the athletic trainer informs the team’s medical staff and the player must be evaluated by the current concussion protocol (see Table). Any player suspected of suffering a concussion is evaluated by the medical staff either on the sideline or in the trainer’s room. The player is given an initial screening containing six signs for obvious disqualification (see Figure) along with a neurological screen for cervical spine injuries and/or serious brain trauma. If the player passes the above they are then evaluated (tablet based) with the Sports Concussion Assessment Tool (version 3), i.e. SCAT-3, and the scores are immediately compared to baseline.8
In addition, in 2013 the NFL instituted a new rule requiring an unaffiliated “neurotrauma consultant,” i.e. neurologist, ER physician or neurosurgeon with an affiliation with a local hospital (the NFL-PA recommended this be a neurologist) be stationed on each sideline to provide a second opinion on the assessment of any potentially concussed players. When a player has been deemed to have suffered a concussion they are immediately removed from play. During the recovery process the player is usually followed by the team’s medical staff and neuropsychologist (who administers follow up computerized, and some cases paper and pencil neuropsychological testing). Once asymptomatic, off of all medications, with a normal neurological exam, and computerized neuropsychological and SCAT-3 testing have returned to baseline, the player is cleared to undergo a graded return to play protocol as outlined in the Zurich Consensus Statement (2012). After the athlete has completed the above they are then required to undergo an evaluation by an independent neurologist that has been approved by the Head, Neck and Spine Committee. When the consulting neurologist, medical team and neuropsychologist are all in agreement the player is then cleared for full contact practice and subsequently for game play.8
STUDIES IN ACTIVE AND RETIRED PLAYERS
Perhaps surprising to an outside observer is the lack of studies in active players. However, most NFL players and professional athletes in general are reluctant to participate in clinical studies for fear the results may be used against them to limit participation, terminate their career, or in contract negotiations.
There are a few retrospective/observational studies including one by Kumar et al.1 who examined the short term effects of concussion on player performance after returning to play. The data was obtained from the NFL (i.e. league profiles) and included injury reports, player age, career experience, games misses and Pro Football Focus performance scores from 2008 to 2012 (which is interesting, because a significant change in NFL concussion management occurred in 2009). One hundred-twenty-four players qualified for the study (defensive secondary, wide receiver, and offensive line were the positions that were most at risk for concussion) and surprisingly 55 percent missed no games after sustaining a concussion. Players that missed at least one game were younger and less experienced; they were also more likely to have sustained a second or repeat concussion (69.5 percent). Older players and players sustaining late season concussions were more likely to return to play without missing any games, with the odd of returning within seven days increasing by 18 percent for each career year, and by 40 percent for each game before the final game of the season. However, the aforementioned odds decreased by 85 percent after the league introduced new concussion guidelines (see above) in 2009 requiring evaluation by an independent neurologist. No difference in player performance was found whether the player did or did not miss a game prior to return to play.1
Recent studies have emerged which support the retired players claims that years of playing professional football has resulted in many developing early dementia. Most have used advanced neuroimaging in conjunction with neuropsychological/ behavioral testing and have found a higher incidence of cognitive issues, depression and white matter abnormalities in retired NFL alumni.
Hart and Didebani6 attempted to correlate cognitive impairment and depression with structural abnormalities on DTI-MRI and blood flow abnormalities using arterial spin labeling and phase contrast MRI. They looked at 34 former NFL players (mean age 61.8), 20 were normal, four had a fixed cognitive deficit, eight MCI, and two dementia (one classified as vascular dementia). Eight (24 percent) were diagnosed as having depression and three of the eight had cognitive difficulties which could not be attributed to depression. Interestingly the researchers were unable to determine concussions/years played and neuropsychological abnormalities. On conventional MRI (i.e. total and deep white matter volumes) there was a significant difference between players with cognitive deficits and age match controls on tests of naming word finding and episodic visual and verbal memory. On DTI imaging NFL players (with cognitive impairment and depression) had statistically significant reductions in fractional anisotropy (FA) in the bilateral frontal/parietal regions as well as the corpus callosum and left temporal lobe when compared to the control group. Regional blood flow differences (left temporal pole, inferior parietal lobe, and superior temporal gyrus) in the cognitively impaired group corresponded to regions associated with impaired neurocognitive performance.6
Two other studies by the same group compared depressive symptoms with white matter dysfunction and the number of concussions.4,5 Both studies used the Beck Depression Inventory version II (BDI-II) and looked at a three factor model of depressive symptoms (affective, cognitive and somatic). The cognitive factor was the only variable that correlated with the number of concussions. However, when using a voxel-wise DTI protocol, there was a negative correlation with FA in the frontal region and total BDI as well as the cognitive and somatic sub-factors, and a partial correlation with the affective sub-factor. There were also negative FA correlations using region of interest (ROI) analysis and total BDI, with FA abnormalities in the forceps minor differentiating depressed from non-depressed athletes.4,5
Our group (in ongoing, unpublished research) has also found deficits on both conventional and DTI-MRI, neuropsychological testing and depression inventories. Of the 10 retired NFL players tested, 50 percent have shown significant abnormalities on DTI-MRI (i.e. FA’s of > 2.5 standard deviations when compared to age matched controls), in the anterior and posterior corona radiata. Thirty percent also had evidence of diffuse axonal injury on conventional MRI (i.e.Gradient Echo and Susceptibility Weighted Imaging). All players with positive MRI findings (i.e. abnormal DTI and/ or conventional imaging) had reported sustaining at least 10 concussions.
Formal neuropsychological testing demonstrated significant abnormalities in attention and concentration (63 percent), executive function (50 percent), learning/memory (50 percent) and spatial/perceptual function (38 percent), which in most players correlated with positive DTI-MRI findings in the regions of interest listed above. Seven out of eight patients were rated as having both depression and anxiety of the MINI International Neuropsychiatric Interview. Functional MRI (fMRI) analysis of retired players looking at brain activation patterns has found pronounced hyperactivation and hypo-connectivity in the dorsolateral and prefrontal cortices which correlated with the number of times a player reported being removed from play after head injury. Surprisingly, computerized neuropsychological testing only showed small differences in executive function in the retired alumni when compared to age matched controls. The results suggest that the athletes have developed cortical compensatory mechanisms (i.e. frontal lobe sub-regions work harder) to counter the neurological impact of repetitive head trauma.3
Contrary to the above studies, Casson et al. used a multivariable analysis, i.e. conventional and DTI-MRI, neuropsychological testing (paper and pencil and computerized), biomarker analysis (APOE4 status) and depression scales (BDI and Patient Health Questionnaire) with the hypothesis that in depth analysis of retired NFL players was unlikely to detect objective clinical abnormalities in a majority of subjects. Of the 45 retired NFL players evaluated 4 (9 percent) had microbleeds, with 3 (7 percent) having a large cavum septum pellucidum with brain atrophy (a possible marker for CTE). The number of concussions was associated with abnormal results of DTI-MRI. Neuropsychological testing revealed isolated impairments in 11 players (24 percent), however none were felt to have dementia. The APOE4 allele (a marker for Alzheimer’s Disease and possibly CTE) was present in 38 percent of the players (a larger number then would be expected in the general male population).2
THE CONCUSSION LAWSUIT
On July 7, 2014 federal judge Anita Brody granted preliminary approval of a settlement between retired NFL players, their family/representatives and the NFL and NFL properties. The retired NFL players sued, accusing the NFL of not warning players and hiding the damages of brain injury. Players and their families do not have to prove that playing professional football caused their injuries. The proposed settlement provides for three benefits: Baseline medical exams (by a neurologist or neuropsychologist) for retired NFL players ($75 million); monetary awards ($765 million and possibly more in total) for diagnoses of ALS (Lou Gehrig’s disease), Alzheimer’s disease (AD), Parkinson’s disease (PD), dementia and certain cases of chronic traumatic encephalopathy or CTE and Education programs and initiatives related to football safety ($10 million).
Retired players had until October 14, 2014 to opt out of the lawsuit with just under 200 doing so. On November 18, 2014 a fairness hearing was held in Philadelphia where judge Brody heard comments and objections to the settlement and to determine whether or not to approve the settlement as fair, reasonable and accurate. Her final decision is pending. Many including myself filed objections (see below).
The settlement recognizes two subclasses of plaintiffs. Those diagnosed with ALS, AD, PD, level 2 cognitive impairment (moderate dementia), level 1.5 cognitive impairment (early dementia), or a pathological diagnosis of CTE before July 7, 2014 and those diagnosed after. Individuals diagnosed prior to the cutoff date will receive higher monetary awards. In order to receive monetary awards retired players with at least one half of an eligibility season will need to undergo a baseline assessment through the baseline assessment program (BAP). The BAP will use a nationwide network of qualified and independent medical providers who will provide the initial baseline assessment as well as any further testing and/or treatment. The BAP Administrator, which will be appointed by the court, will establish the network of medical providers, i.e. neurologists and neuropsychologists.
Providers must be approved by both the NFL lead consul and the co-consul for the retired players and cannot serve as an expert witness for those players who opt out, nor could they have served as an expert witness for the current lawsuit. Criteria for selection includes; education, licensure, credentials, the ability to see players in a timely manner, geographic location, and the ability to provide on-site evaluations as per the BAP. Interestingly, those who elect to forgo being evaluated through the BAP program are still eligible for monetary awards (they appear to be lower), however, will need to be evaluated by board-certified neurologists, board-certified neurosurgeons or board-certified neuro-specialist physician or similarly qualified specialists. Retired players over age 43 have two years from the start of the BAP to undergo a baseline examination, and retired players under age 43 have 10 years. Many players have or are currently undergoing evaluation outside of the BAP.
Current testing (this may change pending full ratification and the development of the BAP) consists of a comprehensive neurological history and exam focusing on the evaluation of the player for dementia, Parkinson’s disease and ALS. We also screen for depression and other mood disorders, sleep disorders and headache. All players receive a mini-mental status examination, clinical dementia rating scale (CDR), and a pre-defined battery of neuropsychological tests (see below), an estimated pre-morbid function (Test of Premorbid Functioning (TOPF)) and current IQ.
There are five domains of cognitive functioning tested. Each domain contains several sub tests. For example, looking at the domain of Complex Attention/Processing Speed, there are six subtests/test scores (digit span, arithmetic, letter number sequencing, coding, cancellation, symbol search, cancellation). Other domains include: executive functioning (four subtests), learning and memory (six subtests), language (three subtests), and visual/perceptual (three subtests).
The scores are then compared to demographically adjusted normative data for Caucasians and African Americans and a standard deviation (SD) below expected norm and a player must have more than one low test score in each domain. The basic principal in defining impairment is that the neuropsychologist or neurologist must determine that a pattern of performance decline has occurred (1.5 SD below expected for level 1 impairment, 1.7-1.8 SD below expected for level 1.5 impairment, or 2 SD for level 2 impairment) below the person’s expected level of premorbid functioning. Complicating things further is the sub tests are actually weighted based on estimated intellectual functioning with those having a below average level of pre-morbid intellectual functioning needed more tests to be abnormal then those with above average functioning.
Alumni also undergo freestanding, embedded and regression based performance validity metrics along with testing for depression (MMPI-2RF and M.I.N.I. Version 5.0.0). Many centers (ours included) also perform a Diffusion Tensor MRI study and an APOE level (neither are required as part of the BAP). Advanced PET scanning and biomarker studies may be incorporated in the future.
A player who is diagnosed with level 1.0 neuroognitive impairment (i.e., moderate cognitive impairment see criteria below), will be eligible to receive further medical testing and/or treatment for what appears to be the next five years. Although the baseline examination can be used as a comparison to measure any subsequent deterioration of cognitive condition over the course of his life there does not appear to be any provisions for continued treatment after the five year period expires unless the patient progresses to the next level of impairment.
Players diagnosed with level 1.5 neurocognitive impairment i.e. early dementia, Level 2 Neurocognitive impairment i.e. moderate dementia, Alzheimer’s disease, Parkinson’s disease, ALS, and CTE (i.e. after death) are eligible for financial awards. These awards are based upon the severity of the disease, number of years played and players age at onset (see table) and range from twenty five thousand dollars to five million dollars. Some have criticized the amounts as being inadequate given the degree of impairment that some players will experience and the amounts awarded to non-athletes who have experienced other types of disability from both work and non-work related accidents.
Some of the biggest criticism has come from Robert Stern, PhD, a neuropsychologist and CTE researcher who has filed an affidavit as part of a larger objection. In his statement he is critical of the lack of testing for behavioral and mood disorders. He notes that several well-known former NFL players (Junior Seau and Dave Duerson) who were diagnosed neuropathologically with CTE did not have signs of dementia and would not have been found impaired under the BAP. There are also concerns over varying degrees of practice by neurologists (i.e. the use or lack of use of biomarkers and advanced neuroimaging) which may result in inaccurate diagnosis.
Some of his biggest criticisms are directed at neuropsychological testing and the use of the CDR, they include; the length of the test battery, more appropriateness of the battery (it is more appropriate for the evaluation of a younger traumatic brain injury patient), use of the M.I.N.I. (which has no bearing on the awards), the validity testing (which can result in false positives in demented individuals), and the subcategories (community affairs, home & hobbies, and personal care) of the CDR used to define Level 1.5 and 2 Neurocognitive Impairment which if met would mean the athlete would be unable to live and function independently. Finally he feels that the algorithm used to translate test performance into compensation is “arbitrary,” “nonstandard”, and “not supported by any scientific literature.”
Complicating things further are newly released guidelines by the International Working Group (IWG) and National Institute on Aging and Alzheimer’s Association (NIA-AA) which to different degrees incorporate the use of biomarkers (i.e. PET imaging, CSF tau and A-Beta protein) in the diagnosis. The NFL lawsuit has no such requirements and many have argued that individuals with positive biomarkers have met the criteria for AD. Overall the NFL diagnostic criteria most closely resembles the NIA-AA classification which breaks the diagnoses into a pre-clinical component, mild cognitive impairment (MCI) and AD dementia. Unlike the NFL criteria which make the diagnosis when the retired athlete has exhibited significant cognitive decline , the IWG guidelines focus on the early diagnosis of Alzheimer’s disease. They also rely on a more focused and simplified neuropsychological battery focusing on impaired performance on episodic memory testing. The IWG recommendations have diagnostic criteria for atypical AD and its associated phenotypes (occiptotemoral, biparietal, frontal, Logoenic) whereas the NFL does not.
Over the past five years the NFL and NFL-PA have made significant strides in improving player safety when it comes to head injuries. This has included expanding sideline medical personnel, adding an independent neurological consultant, rule changes i.e. helmet to helmet contact, and perhaps most important, player education. With that said, there is still significant room for improvement especially when it comes to the role of neurologists. Unfortunately, it may be too late for many retired players who are now showing signs of early dementia and some even ALS and Parkinson’s disease. Unlike in the past when the field essentially ignored sports related head injury, neurologists along with the American Academy of Neurology and subspecialty organizations need to step to the forefront when it comes the evaluating and managing these individuals a majority of who do not have access to basic neurological care. The neurological community also needs to take lead on research, especially longitudinal studies looking at symptom definition and progression, neuro-pathological characteristics, advanced neuroimaging and other biomarkers, as well as evidence based treatment options.
Francis X. Conidi, DO, is the Director of the Florida Center for Headache and Sports Neurology.
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