Journal of the Neurological Sciences 356 (2015) 97–101
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Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Evaluation of the King–Devick test as a concussion screening tool in high school football players Daniel H. Seidman a, Jennifer Burlingame a, Lina R. Yousif a, Xinh P. Donahue a, Joshua Krier a, Lydia J. Rayes a, Rachel Young a, Muareen Lilla b, Rochelle Mazurek b, Kristie Hittle b, Charles McCloskey a, Saroj Misra a, Michael K. Shaw c,⁎ a b c
Department of Family Medicine, St. John Macomb-Oakland Hospital, St. John Providence Health System, United States Department of Physical Rehabilitation, St. John Macomb-Oakland Hospital, St. John Providence Health System, United States Department of Medical Education and Research, St. John Macomb-Oakland Hospital, St. John Providence Health System, United States
a r t i c l e
i n f o
Article history: Received 20 November 2014 Received in revised form 10 June 2015 Accepted 11 June 2015 Available online 12 June 2015 Keywords: Traumatic brain injury Diffuse axonal injury Neuropsychological tests Post-concussion syndrome Visual motor coordination Football
a b s t r a c t Objective: Concussion is the most common type of traumatic brain injury, and results from impact or impulsive forces to the head, neck or face. Due to the variability and subtlety of symptoms, concussions may go unrecognized or be ignored, especially with the pressure placed on athletes to return to competition. The King–Devick (KD) test, an oculomotor test originally designed for reading evaluation, was recently validated as a concussion screening tool in collegiate athletes. A prospective study was performed using high school football players in an attempt to study the KD as a concussion screening tool in this younger population. Methods: 343 athletes from four local high school football teams were recruited to participate. These athletes were given baseline KD tests prior to competition. Individual demographic information was collected on the subjects. Standard team protocol was employed to determine if a concussion had occurred during competition. Immediately after diagnosis, the KD test was re-administered to the concussed athlete for comparison to baseline. Post-season testing was also performed in non-concussed individuals. Results: Of the 343 athletes, nine were diagnosed with concussions. In all concussed players, cumulative read times for the KD test were significantly increased (p b 0.001). Post-season testing of non-concussed athletes revealed minimal change in read times relative to baseline. Univariate analysis revealed that history of concussion was the only demographic factor predictive of concussion in this cohort. Conclusion: The KD test is an accurate and easily administered sideline screening tool for concussion in adolescent football players. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Concussion is the most common type of traumatic brain injury, and results from impact or impulsive forces to the head, neck or face. Athletes in certain contact sports may be especially vulnerable to concussion [1]. Symptoms can include amnesia or loss of consciousness, and symptomatic changes in three areas: physical (drowsiness, loss of balance, weakness in extremities), cognitive (feeling in a fog, slurred speech), and emotional (irritability) [2,3]. Due to the variability and subtlety of symptoms, concussions may be unrecognized or even ignored, especially with the pressure placed on athletes to return to Abbreviations: KD, King–Devick; ImPACT, immediate post-concussion and cognitive testing; MACE, military acute concussion evaluation; LOC, loss of consciousness; SCAT, sport concussion assessment tool; SAC, standardized assessment of concussion; PCSS, post-concussion symptom scale; SAC, standardized assessment of concussion. ⁎ Corresponding author at: St. John Macomb-Oakland Hospital, 12001 E. Twelve Mile Road, Warren, MI 48093, United States. E-mail address: [email protected] (M.K. Shaw).
http://dx.doi.org/10.1016/j.jns.2015.06.021 0022-510X/© 2015 Elsevier B.V. All rights reserved.
competition. As demonstrated in animal models [4,5], and suggested in human studies [6,7], athletes who have had one concussion may be susceptible to another, especially if the new injury occurs before symptoms from the previous concussion has completely resolved. A phenomenon known as second impact syndrome [6,8], while rare, is also a risk of repetitive concussion. The neurobiology of concussion has been described by Giza et al. as a neuro-metabolic cascade of events that involves bio-energetic challenges, cytoskeletal and axonal alterations, impairments in neurotransmission, vulnerability to delayed cell death and chronic dysfunction. In the acute setting, this increased demand for energy occurs in a setting of normal or reduced cerebral blood flow, resulting in an uncoupling, or mismatch, between energy supply and demand [9]. Sport-related concussion has received increased scrutiny recently with the realization that repetitive brain injury may lead to consequences later in life — including anxiety, depressive disorders and chronic traumatic encephalopathy (CTE). Per Gardner et al., CTE has recently been redefined from the original condition resembling Alzheimer's disease in
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D.H. Seidman et al. / Journal of the Neurological Sciences 356 (2015) 97–101
professional boxers to a new condition observed in athletes and others that shares many features with known psychiatric disorders and other forms of dementia [10]. It has also been realized that prompt diagnosis of sport-related concussion can allow athletes to be removed from competition for recovery, potentially preventing long-term sequelae of repetitive head trauma [11,12]. The King–Devick (KD) test was recently validated as an accurate and reliable concussion screening test in mixed martial arts fighters, rugby players and collegiate athletes [13–15]. Originally designed as an oculomotor test for reading evaluation, the KD test is based on performing rapid number naming which requires eye movements, concentration, attention and language [14]. The test subject reads a series of numbers in right-to-left and up-to-down order on three test cards. The test is available in a physical spiral bound test or electronic iPad application. The accuracy of the reading and the time taken to read the cards is recorded. A baseline is established and used for comparison. Worsening of cumulative read time from baseline has been noted in players diagnosed with concussion [13–16]. The test can be administered on the sideline during competition in less than 2 min, by a layperson [17], and may aid in the detection of athletes with concussion. 2. Methods 337 varsity football players from four Southeast Michigan high schools were enrolled in this prospective study, which took place during the Fall 2013 season. The St. John Providence Health System IRB committee approved the study. All participants signed a written consent to be a part of the study. If participants were minors at the time of enrollment, written consent by their parent/legal guardian was obtained along with assent of the minor. The administration and head coaches of each of the high schools approved participation in the study. Inclusion criteria included all high school athletes from participating schools participating in football. Subjects were willing and able to give informed consent according to the guidelines established by the St. John IRB or those minors with signed informed consent from their parent or legal guardian. Subjects were excluded from the study if their English language skills were insufficient to understand the written informed consent or the testing procedures. Athletes with diagnosed reading difficulties were also excluded from the study. Two athletes with diagnosed dyslexia were thus excluded. Permission to use the King–Devick test was purchased from the King–Devick Test Inc. (Oakbrook Terrace, IL). The KD test consists of a series of three numbered cards that the participant reads while being timed. The cumulative read time of all three cards was recorded as a baseline measurement. The KD tested was administered by a research team consisting of athletic trainers, physicians, scientists and medical students, all of whom received prior training on test administration. These trained personnel were routinely available for testing at each practice and game during the season. Baseline tests were administered at a team practice to simulate the noisy sideline environment that would be encountered during competition. The test maker's recommendations for baseline testing were followed. In brief, the athlete was asked to read each test card as quickly as possible without making an error. If an error was made that was not quickly corrected, the test was restarted. The fastest cumulative test time of two attempts was recorded as the athlete's baseline time. Individual demographic information on the subjects was collected as well. Concussion history was self-reported by answering ‘yes’ to the question ‘Have you ever been diagnosed with a concussion?’ All four teams employed ImPACT testing as part of their concussion policy. Although ImPACT testing can be utilized with normative values for this age group, baseline testing was conducted instead as it has been suggested that this is preferable [18]. Since ImPACT testing is not designed for sideline evaluation of concussion, in the event of an on-field injury, standard team practice was employed to determine if a concussion had occurred. St. John Providence Sports Medicine concussion policy is based upon the
recommendations of the Concussion in Sport Group (CISG) first position statement and subsequent statements [1]. In general, concussion was evaluated when an athlete presented with a mechanism of injury—direct or indirect forces to the head, neck or face. Forces may include direct forces with the ground, another player, or other objects in the playing area; indirect forces are most common with whiplash type injuries such as a blow to the shoulders. If an injury mechanism existed, then the tests of the SCAT3 assessment tool were employed by the medical professional present to assess for concussion. Diagnosis of concussion was left to the professional with all diagnosed athletes having a deficit of at least 30% on SCAT3 tests. All athletes diagnosed in this manner were subsequently tested with ImPACT within 72 h of the event. Study personnel were on field for all practices and games to assure prompt KD testing of diagnosed players. After on-field concussion diagnosis, the KD test was re-administered to all injured athletes within 30 min of removal from play, and the scores were recorded for comparison to baseline. Time, date, and symptomatology were also noted. At the end of the season, the KD test was re-administered to all players to determine the extent of learning effects as well as any deviation from baseline. This testing was again done on the sidelines during a game-like practice session. Descriptive statistics were generated to characterize the study populations with respect to demographic factors such as age, weight, height, race and position played. Continuous variables were described using the mean ± standard deviation. Categorical variables were described using frequency distributions. Univariate between group comparisons were performed using Chi squared tests for categorical variables. The normality of distribution was tested using the Shapiro– Wilk test. For comparison of read times, non-parametric statistical tests were used given the small sample size (n = 9) for athletes with concussion and sideline testing. Differences in KD time scores from pre- to post-season were calculated, and pre- and post-season KD scores were compared within athletes using the Wilcoxon signed-rank test. For athletes with concussion, sideline KD scores were compared similarly with pre-season baseline scores. Logistic regression analysis was performed to determine predictors, if any, of concussion by study group, age, gender, and other collected factors. All statistical analyses were performed using SPSS v. 22.0. A two tailed p-value of 0.05 or less was considered to indicate statistical significance. 3. Results Demographic data for the concussed and non-concussed cohorts is shown in Table 1. The population of high school football athletes Table 1 Study population demographics.
n Ethnicity Caucasian African American Other Age (years) Height (inches) Height (centimeters) Weight (pounds) Weight (kilograms) History of concussion Player position Lineman Defensive back Wide receiver Linebacker Running back Quarterback Kicker
Players without concussion
Players with concussion
328
9
236 (72%) 79 (24%) 13 (4%) 15.4 ± 1.3 69.8 ± 3.4 177.3 ± 8.6 175.6 ± 42.2 79.7 ± 19.1 26 (8%)
9 (100%) 0 0 15.6 ± 1.0 71.7 ± 3.8 182.1 ± 9.7 179.1 ± 29.3 81.2 ± 13.3 4 (44%)
134 (41%) 45 (14%) 62 (19%) 41 (13%) 29 (9%) 15 (5%) 2 (.6%)
3 (33%) 2 (22%) 1 (11%) 1 (11%) 1 (11%) 1 (11%) 0
p value
0.63
0.65 0.11 0.80 0.002 1.0 .63 1.0 1.0 .58 .38 1.0
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consisted of 337 subjects, of which 9 (2.7%) were diagnosed with a concussion during competition or practice. Clinical symptoms of concussion were noted in all 9 players. Two players had temporary loss of consciousness. As assessed by SCAT3, all concussed players were disoriented and had balance difficulties, and five of the nine experienced memory loss. With respect to concussed and non-concussed players, there was no significant difference between the ethnicity (p = 0.63), age (p = 0.65), height (p = 0.11), or weight (p = 0.80) of our subjects (Table 1). However, 4 of 9 (44.4%) of athletes who sustained concussion in the football season had a history of concussion compared with only 26 of 328 (7.9%) non-concussed athletes (p = 0.002). No significant differences were seen in any measured point between players with and without previous concussion. Of note, all of the athletes who had previously sustained concussion were asymptomatic and cleared for return to play prior to this study. Sideline KD test times were significantly worse (higher) compared to baseline among concussed players as displayed in Table 2 (median 66.2 s sideline vs. 47.2 s baseline, p b 0.001). Slowing of the cumulative read times as compared to baseline resulted in a time delta of 148.2%. This increased read time was seen in each of the individual cards and was statistically significant for each individual card. The first card, which is comparably easiest to read, had the greatest change in read time. Errors in the reading of the cards (missed numbers or incorrectly identified numbers) were few and present only in two of the nine concussed players (data not shown). Comparison of pre- and post-season KD testing times of nonconcussed athletes (Table 2) revealed a minimal improvement (decrease) in median read time (47.4 ± 9.7 vs. 46.8 ± 11.5, delta of 1.3%), although this improvement was not statistically significant (p = 0.73). Each individual athlete with concussion demonstrated worsening of cumulative read times (Table 3). The increase from baseline KD testing ranged from 9.5 s (114.6% of baseline) to 44.6 s (193.9% of baseline). End of season retesting of these athletes revealed that in 6 of the 7 who did not drop out of football, their cumulative read times had returned to near baseline (Table 3). 4. Discussion The results of this study demonstrate that the KD test is an accurate and easily administered sideline screening tool for concussion in adolescent football players. Players who suffered concussions were shown to have significantly increased read times relative to baseline. The group that sustained the most concussions was lineman (n = 3) followed by defensive backs (n = 2), and one concussion each for the positions of wide receiver, linebacker, running back, and quarterback. This observation may be due to the likelihood or force of impact per position and further research may be useful in determining why this is the case. A study by Baugh et al. has shown that, while the number of concussion doesn't seem to vary by position, the number of self-reported post-impact symptoms is highest in offensive linemen [19]. As stated above, a significant number of concussed players had a history of concussion (44%). This is not surprising, since a propensity for concussion
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in those with a history of this injury has been well documented in the literature [6,7]. This is also important to note because of possible longterm neuropsychiatric consequences currently being investigated, such as altered cognition, depression, chronic traumatic encephalopathy, and Alzheimer's disease [2,3,6,8]. In this study, there was a range of 14.6% to 110.3% increase in cumulative read time from baseline. It is known that concussions can range in severity and exhibit a variety of symptoms. This large range in the concussed players may be explained by the unique severity of each player's concussion. Future study is recommended to investigate correlation between the amount of time worsening from baseline and severity of concussion injury. In the absence of concussion, previous investigations of MMA fighters [15], rugby players [13,20,21], and college athletes [14], revealed that the KD test has “learning effects” associated with repeated testing. Galetta and colleagues hypothesized that this effect accounted for many athletes improving (decreasing) their KD times over the course of two testing sessions or between pre- and post-season measurements. While our investigation did reveal some degree of learning effect, the difference was modest compared to other studies and was not statistically significant (p = 0.73) (Table 2). This difference may be specific for younger athletes, or may be due to differences in interval between pre- and post-season testing. For instance, MMA fighters were exposed to the KD test three times in one day. In this study, time between pre- and post-season testing of concussed athletes was consistent and of substantial duration, 12 weeks, owing to the uniform high school football season in Michigan. Currently, the SCAT3 is one of the most widely utilized tools to aid in the diagnosis of concussion. In recent years ImPACT testing has been shown to also play a role in monitoring visual motor speed, reaction time, and verbal and visual memory. Each of these has been recognized as an area of impairment in concussion. The ImPACT test is the current standard used by the participating high schools for assessing concussion-related symptoms and is also utilized by the NCAA and several professional sports. It is the most widely used and validated test for assessing baseline function and return to play [1]. However, it is cumbersome in that testing requires approximately 30 min, a computer, a quiet environment, and a licensed administrator. The KD test has already been validated as a rapid sideline screening tool as discussed above [13–15]. Tjarks et al.'s study on ImPACT testing versus KD testing shows that the KD test effectively assesses recovery of oculomotor speed and visual processing which are some of the more commonly reported symptoms of concussed patients [22]. With further investigation, the KD test may gain validation as a tool for concussion detection and may be utilized in assessing a player's recovery of cognitive function, similar to the PCSS and ImPACT tests. Determining a player's return to full activity after a concussion, although still a clinical decision, has been aided by ImPACT testing. All of the high school football players in this study received baseline and post-concussion ImPACT testing in addition to King–Devick testing. It has previously been shown that the KD and ImPACT tests correlate with respect to concussion diagnosis and return to baseline function following a concussion [22]. KD performance significantly correlated with the visual motor speed/memory and reaction time components of the
Table 2 Read times.
Players with Concussion
Players without concussion
Card 1 Card 2 Card 3 Cumulative total Card 1 Card 2 Card 3 Cumulative total
Baseline tests median time in seconds (range)
Sideline tests median time in seconds (range)
Delta
p value
14.2 (10.5–18.4) 15.6 (11.4–19.2) 17.3 (11.4–19.2) 47.1 (33.3–67.5) 14.7 (9.1–26.5) 15.1 (9.7–28.9) 16.5 (9.7–41.4) 47.4 ± 9.7
22.0 (16.0–28.1) 21.2 (17.3–29.9) 24.3 (16.0–36.9) 66.2 (51.0–72.1) 14.1 (9.3–26.2) 14.9 (9.3–27.8) 16.4 (10.1–40.3) 46.8 ± 11.5
154.9% 135.9% 140.5% 140.6% 95.5% 98.7% 99.4% 98.7%
0.001 0.0008 0.004 0.003 0.50 0.31 0.80 0.73
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Table 3 Individual players with concussion.
Player 1 Player 2 Player 3 Player 4 Player 5 Player 6 Player 7 Player 8 Player 9
Baseline cumulative read time (s)
Sideline cumulative read time (s)
Sideline percent baseline (%)
Repeat (end of season) read time (s)
End of season percent baseline
42.4 44.5 58.3 35.0 47.5 59.1 43.3 47.1 54.7
65.7 51.0 89.9 73.6 92.1 90.2 56.4 54.1 66.2
155.0 114.6 154.2 210.3 193.9 152.6 130.3 114.9 121.0
42.1 43.7 61.8 60.6 60.8 58.4 42.9 NA NA
99.3% 98.2% 106.0% 173.1% 128% 98.8% 99.2% – –
NA = lost to follow-up (quit football)
ImPACT test after a concussion. This helps to demonstrate that KD may be a useful sideline screen for concussion in addition to a useful tool in monitoring recovery in the high school football player. In this study, there was circumstantial evidence that as symptoms resolved, both ImPACT scores improved and KD testing times decreased (improved). Seven of the nine concussed athletes were tested at season's end per protocol, (two of the nine concussed players were lost to follow-up). One player with residual cognitive deficit at season's end, as assessed by ImPACT testing, also had significantly slower read times on the KD test. The other re-tested players, who were cleared to play following ImPACT testing, had no residual deficit as assessed by KD testing. This suggests that, with further research, KD test may have value as a return to play test. A prior study on MMA fighters attempted to define a standardized percent increase that may define concussion using KD testing [15]. This was partly based on the fact that fighters who lost consciousness had even higher KD read times than those who suffered concussion without LOC. KD scores were also shown to correlate with PCSS and MACE scores after concussion. The authors of this paper suggested that a 5 s worsening in cumulative KD times was indicative of concussion, but this difference in time has not been further defined in other studies. In this study, the minimal increase in cumulative read time in a concussed player was 6.5 s (14%) above baseline, which fits with this hypothesis. However, no non-concussed athlete had increased (worse) post-season KD times compared to baseline, suggesting that any increase in cumulative read time was indicative of concussion in this specific cohort as indicated in the instructions for the KD test. Concussed patients exhibit a varied number of symptoms that can sometimes be difficult to diagnose at the time of injury. The KD test offers objective assessment of rapid eye movement, language, and attention that may help screen for concussion at the time of head trauma. This is significant because early diagnosis of concussion leading to removing a player from play is crucial to protecting their brain health [23]. KD testing offers the ability to efficiently and accurately screen players on the sidelines who may have suffered a concussion and quickly determine that they be removed from play until a comprehensive diagnosis can be made. Several limitations were encountered through the course of this research. First, the sample size of concussed athletes was smaller than anticipated, which creates some difficulty with respect to generalizing conclusions reached in this study. It is possible that the use of SCAT3 on field and ImPACT testing after injury to verify concussion may be a more a stringent set of criteria for diagnosis than used in other studies. Also, in the state of Michigan, there has been a dramatic increase in concussion awareness among high school athletes and their parents, coaches and medical personnel working with the sports teams. This results from educational efforts mandated by recent legislation in the state. It is possible that coaches have helped to lower concussion rates as they emphasize proper tackling and blocking techniques and players learn that “leading with your head” has health consequences. Paradoxically, this education could also lead to an under reporting of symptoms by the players as they come to realize that the diagnosis of concussion
mandates removal from play. This sentiment was expressed by a number of players during interviews for the study and has been reported previously [24]. One of the strengths of this study comes from the fact that none of the concussed players experienced vision difficulties. Kontos et al. states that vision difficulties are reported in 30% of concussed individuals [25], which may affect the sensitivity of the KD as a screening tool. This further strengthens the case for a multifaceted diagnostic process [26]. This study supports existing evidence that the KD test is effective in youth sports because it can be used by a trained layperson such as a coach, teacher, or volunteer, takes only minutes to perform, and can be administered easily at the sidelines due to its portable nature. Having such a tool is essential in contact sports where third party pressures to return to play without physician evaluation are ever-present. Future studies may show the KD test to be a useful screening tool in other youth sports and perhaps on the professional level as well. Conflicts of interest None. Acknowledgments The authors would like to thank the following individuals for their contributions: Allison Blumenthal BS, Scott Mueller BS, Collin Blattner BS, Logan McCool BS, Jacqueline Dufour BS, and Mary Predko BS. We would like to acknowledge the Medical Executive Committee at St. John Macomb-Oakland Hospital for their financial support of these research efforts. We would also like to acknowledge all of the high school football coaches and administrators who allowed us access to the athletes throughout the football season. Finally, we would like to acknowledge the athletes and their parents for their participation in this study. References [1] M. Aubry, R. Cantu, J. Dvorak, T. Graf-Baumann, K. Johnston, J. Kelly, M. Lovell, P. McCrory, W. Meeuwisse, P. Schamasch, Summary and agreement statement of the First International Conference on Concussion in Sport, Vienna 2001. Recommendations for the improvement of safety and health of athletes who may suffer concussive injuries, Br. J. Sports Med. 36 (2002) 6–10. [2] K.G. Harmon, J.A. Drezner, M. Gammons, K.M. Guskiewicz, M. Halstead, S.A. Herring, J.S. Kutcher, A. Pana, M. Putukian, W.O. Roberts, American Medical Society for Sports Medicine position statement: concussion in sport, Br. J. Sports Med. 47 (2013) 15–26. [3] N.A. Shaw, The neurophysiology of concussion, Prog. Neurobiol. 67 (2002) 281–344. [4] H.L. Laurer, F.M. Bareyre, V.M. Lee, J.Q. Trojanowski, L. Longhi, R. Hoover, K.E. Saatman, R. Raghupathi, S. Hoshino, M.S. Grady, T.K. McIntosh, Mild head injury increasing the brain's vulnerability to a second concussive impact, J. Neurosurg. 95 (2001) 859–870. [5] L. Longhi, K.E. Saatman, S. Fujimoto, R. Raghupathi, D.F. Meaney, J. Davis, B.S.A. McMillan, V. Conte, H.L. Laurer, S. Stein, N. Stocchetti, T.K. McIntosh, Temporal window of vulnerability to repetitive experimental concussive brain injury, Neurosurgery 56 (2005) 364–374. [6] N.M. Wetjen, M.A. Pichelmann, J.L. Atkinson, Second impact syndrome: concussion and second injury brain complications, J. Am. Coll. Surg. 211 (2010) 553–557. [7] C.M. Baugh, J.M. Stamm, D.O. Riley, B.E. Gavett, M.E. Shenton, A. Lin, C.J. Nowinski, R.C. Cantu, A.C. McKee, R.A. Stern, Chronic traumatic encephalopathy: neurodegeneration
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Contents lists available at ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Evaluation of the King–Devick test as a concussion screening tool in high school football players Daniel H. Seidman a, Jennifer Burlingame a, Lina R. Yousif a, Xinh P. Donahue a, Joshua Krier a, Lydia J. Rayes a, Rachel Young a, Muareen Lilla b, Rochelle Mazurek b, Kristie Hittle b, Charles McCloskey a, Saroj Misra a, Michael K. Shaw c,⁎ a b c
Department of Family Medicine, St. John Macomb-Oakland Hospital, St. John Providence Health System, United States Department of Physical Rehabilitation, St. John Macomb-Oakland Hospital, St. John Providence Health System, United States Department of Medical Education and Research, St. John Macomb-Oakland Hospital, St. John Providence Health System, United States
a r t i c l e
i n f o
Article history: Received 20 November 2014 Received in revised form 10 June 2015 Accepted 11 June 2015 Available online 12 June 2015 Keywords: Traumatic brain injury Diffuse axonal injury Neuropsychological tests Post-concussion syndrome Visual motor coordination Football
a b s t r a c t Objective: Concussion is the most common type of traumatic brain injury, and results from impact or impulsive forces to the head, neck or face. Due to the variability and subtlety of symptoms, concussions may go unrecognized or be ignored, especially with the pressure placed on athletes to return to competition. The King–Devick (KD) test, an oculomotor test originally designed for reading evaluation, was recently validated as a concussion screening tool in collegiate athletes. A prospective study was performed using high school football players in an attempt to study the KD as a concussion screening tool in this younger population. Methods: 343 athletes from four local high school football teams were recruited to participate. These athletes were given baseline KD tests prior to competition. Individual demographic information was collected on the subjects. Standard team protocol was employed to determine if a concussion had occurred during competition. Immediately after diagnosis, the KD test was re-administered to the concussed athlete for comparison to baseline. Post-season testing was also performed in non-concussed individuals. Results: Of the 343 athletes, nine were diagnosed with concussions. In all concussed players, cumulative read times for the KD test were significantly increased (p b 0.001). Post-season testing of non-concussed athletes revealed minimal change in read times relative to baseline. Univariate analysis revealed that history of concussion was the only demographic factor predictive of concussion in this cohort. Conclusion: The KD test is an accurate and easily administered sideline screening tool for concussion in adolescent football players. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Concussion is the most common type of traumatic brain injury, and results from impact or impulsive forces to the head, neck or face. Athletes in certain contact sports may be especially vulnerable to concussion [1]. Symptoms can include amnesia or loss of consciousness, and symptomatic changes in three areas: physical (drowsiness, loss of balance, weakness in extremities), cognitive (feeling in a fog, slurred speech), and emotional (irritability) [2,3]. Due to the variability and subtlety of symptoms, concussions may be unrecognized or even ignored, especially with the pressure placed on athletes to return to Abbreviations: KD, King–Devick; ImPACT, immediate post-concussion and cognitive testing; MACE, military acute concussion evaluation; LOC, loss of consciousness; SCAT, sport concussion assessment tool; SAC, standardized assessment of concussion; PCSS, post-concussion symptom scale; SAC, standardized assessment of concussion. ⁎ Corresponding author at: St. John Macomb-Oakland Hospital, 12001 E. Twelve Mile Road, Warren, MI 48093, United States. E-mail address: [email protected] (M.K. Shaw).
http://dx.doi.org/10.1016/j.jns.2015.06.021 0022-510X/© 2015 Elsevier B.V. All rights reserved.
competition. As demonstrated in animal models [4,5], and suggested in human studies [6,7], athletes who have had one concussion may be susceptible to another, especially if the new injury occurs before symptoms from the previous concussion has completely resolved. A phenomenon known as second impact syndrome [6,8], while rare, is also a risk of repetitive concussion. The neurobiology of concussion has been described by Giza et al. as a neuro-metabolic cascade of events that involves bio-energetic challenges, cytoskeletal and axonal alterations, impairments in neurotransmission, vulnerability to delayed cell death and chronic dysfunction. In the acute setting, this increased demand for energy occurs in a setting of normal or reduced cerebral blood flow, resulting in an uncoupling, or mismatch, between energy supply and demand [9]. Sport-related concussion has received increased scrutiny recently with the realization that repetitive brain injury may lead to consequences later in life — including anxiety, depressive disorders and chronic traumatic encephalopathy (CTE). Per Gardner et al., CTE has recently been redefined from the original condition resembling Alzheimer's disease in
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professional boxers to a new condition observed in athletes and others that shares many features with known psychiatric disorders and other forms of dementia [10]. It has also been realized that prompt diagnosis of sport-related concussion can allow athletes to be removed from competition for recovery, potentially preventing long-term sequelae of repetitive head trauma [11,12]. The King–Devick (KD) test was recently validated as an accurate and reliable concussion screening test in mixed martial arts fighters, rugby players and collegiate athletes [13–15]. Originally designed as an oculomotor test for reading evaluation, the KD test is based on performing rapid number naming which requires eye movements, concentration, attention and language [14]. The test subject reads a series of numbers in right-to-left and up-to-down order on three test cards. The test is available in a physical spiral bound test or electronic iPad application. The accuracy of the reading and the time taken to read the cards is recorded. A baseline is established and used for comparison. Worsening of cumulative read time from baseline has been noted in players diagnosed with concussion [13–16]. The test can be administered on the sideline during competition in less than 2 min, by a layperson [17], and may aid in the detection of athletes with concussion. 2. Methods 337 varsity football players from four Southeast Michigan high schools were enrolled in this prospective study, which took place during the Fall 2013 season. The St. John Providence Health System IRB committee approved the study. All participants signed a written consent to be a part of the study. If participants were minors at the time of enrollment, written consent by their parent/legal guardian was obtained along with assent of the minor. The administration and head coaches of each of the high schools approved participation in the study. Inclusion criteria included all high school athletes from participating schools participating in football. Subjects were willing and able to give informed consent according to the guidelines established by the St. John IRB or those minors with signed informed consent from their parent or legal guardian. Subjects were excluded from the study if their English language skills were insufficient to understand the written informed consent or the testing procedures. Athletes with diagnosed reading difficulties were also excluded from the study. Two athletes with diagnosed dyslexia were thus excluded. Permission to use the King–Devick test was purchased from the King–Devick Test Inc. (Oakbrook Terrace, IL). The KD test consists of a series of three numbered cards that the participant reads while being timed. The cumulative read time of all three cards was recorded as a baseline measurement. The KD tested was administered by a research team consisting of athletic trainers, physicians, scientists and medical students, all of whom received prior training on test administration. These trained personnel were routinely available for testing at each practice and game during the season. Baseline tests were administered at a team practice to simulate the noisy sideline environment that would be encountered during competition. The test maker's recommendations for baseline testing were followed. In brief, the athlete was asked to read each test card as quickly as possible without making an error. If an error was made that was not quickly corrected, the test was restarted. The fastest cumulative test time of two attempts was recorded as the athlete's baseline time. Individual demographic information on the subjects was collected as well. Concussion history was self-reported by answering ‘yes’ to the question ‘Have you ever been diagnosed with a concussion?’ All four teams employed ImPACT testing as part of their concussion policy. Although ImPACT testing can be utilized with normative values for this age group, baseline testing was conducted instead as it has been suggested that this is preferable [18]. Since ImPACT testing is not designed for sideline evaluation of concussion, in the event of an on-field injury, standard team practice was employed to determine if a concussion had occurred. St. John Providence Sports Medicine concussion policy is based upon the
recommendations of the Concussion in Sport Group (CISG) first position statement and subsequent statements [1]. In general, concussion was evaluated when an athlete presented with a mechanism of injury—direct or indirect forces to the head, neck or face. Forces may include direct forces with the ground, another player, or other objects in the playing area; indirect forces are most common with whiplash type injuries such as a blow to the shoulders. If an injury mechanism existed, then the tests of the SCAT3 assessment tool were employed by the medical professional present to assess for concussion. Diagnosis of concussion was left to the professional with all diagnosed athletes having a deficit of at least 30% on SCAT3 tests. All athletes diagnosed in this manner were subsequently tested with ImPACT within 72 h of the event. Study personnel were on field for all practices and games to assure prompt KD testing of diagnosed players. After on-field concussion diagnosis, the KD test was re-administered to all injured athletes within 30 min of removal from play, and the scores were recorded for comparison to baseline. Time, date, and symptomatology were also noted. At the end of the season, the KD test was re-administered to all players to determine the extent of learning effects as well as any deviation from baseline. This testing was again done on the sidelines during a game-like practice session. Descriptive statistics were generated to characterize the study populations with respect to demographic factors such as age, weight, height, race and position played. Continuous variables were described using the mean ± standard deviation. Categorical variables were described using frequency distributions. Univariate between group comparisons were performed using Chi squared tests for categorical variables. The normality of distribution was tested using the Shapiro– Wilk test. For comparison of read times, non-parametric statistical tests were used given the small sample size (n = 9) for athletes with concussion and sideline testing. Differences in KD time scores from pre- to post-season were calculated, and pre- and post-season KD scores were compared within athletes using the Wilcoxon signed-rank test. For athletes with concussion, sideline KD scores were compared similarly with pre-season baseline scores. Logistic regression analysis was performed to determine predictors, if any, of concussion by study group, age, gender, and other collected factors. All statistical analyses were performed using SPSS v. 22.0. A two tailed p-value of 0.05 or less was considered to indicate statistical significance. 3. Results Demographic data for the concussed and non-concussed cohorts is shown in Table 1. The population of high school football athletes Table 1 Study population demographics.
n Ethnicity Caucasian African American Other Age (years) Height (inches) Height (centimeters) Weight (pounds) Weight (kilograms) History of concussion Player position Lineman Defensive back Wide receiver Linebacker Running back Quarterback Kicker
Players without concussion
Players with concussion
328
9
236 (72%) 79 (24%) 13 (4%) 15.4 ± 1.3 69.8 ± 3.4 177.3 ± 8.6 175.6 ± 42.2 79.7 ± 19.1 26 (8%)
9 (100%) 0 0 15.6 ± 1.0 71.7 ± 3.8 182.1 ± 9.7 179.1 ± 29.3 81.2 ± 13.3 4 (44%)
134 (41%) 45 (14%) 62 (19%) 41 (13%) 29 (9%) 15 (5%) 2 (.6%)
3 (33%) 2 (22%) 1 (11%) 1 (11%) 1 (11%) 1 (11%) 0
p value
0.63
0.65 0.11 0.80 0.002 1.0 .63 1.0 1.0 .58 .38 1.0
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consisted of 337 subjects, of which 9 (2.7%) were diagnosed with a concussion during competition or practice. Clinical symptoms of concussion were noted in all 9 players. Two players had temporary loss of consciousness. As assessed by SCAT3, all concussed players were disoriented and had balance difficulties, and five of the nine experienced memory loss. With respect to concussed and non-concussed players, there was no significant difference between the ethnicity (p = 0.63), age (p = 0.65), height (p = 0.11), or weight (p = 0.80) of our subjects (Table 1). However, 4 of 9 (44.4%) of athletes who sustained concussion in the football season had a history of concussion compared with only 26 of 328 (7.9%) non-concussed athletes (p = 0.002). No significant differences were seen in any measured point between players with and without previous concussion. Of note, all of the athletes who had previously sustained concussion were asymptomatic and cleared for return to play prior to this study. Sideline KD test times were significantly worse (higher) compared to baseline among concussed players as displayed in Table 2 (median 66.2 s sideline vs. 47.2 s baseline, p b 0.001). Slowing of the cumulative read times as compared to baseline resulted in a time delta of 148.2%. This increased read time was seen in each of the individual cards and was statistically significant for each individual card. The first card, which is comparably easiest to read, had the greatest change in read time. Errors in the reading of the cards (missed numbers or incorrectly identified numbers) were few and present only in two of the nine concussed players (data not shown). Comparison of pre- and post-season KD testing times of nonconcussed athletes (Table 2) revealed a minimal improvement (decrease) in median read time (47.4 ± 9.7 vs. 46.8 ± 11.5, delta of 1.3%), although this improvement was not statistically significant (p = 0.73). Each individual athlete with concussion demonstrated worsening of cumulative read times (Table 3). The increase from baseline KD testing ranged from 9.5 s (114.6% of baseline) to 44.6 s (193.9% of baseline). End of season retesting of these athletes revealed that in 6 of the 7 who did not drop out of football, their cumulative read times had returned to near baseline (Table 3). 4. Discussion The results of this study demonstrate that the KD test is an accurate and easily administered sideline screening tool for concussion in adolescent football players. Players who suffered concussions were shown to have significantly increased read times relative to baseline. The group that sustained the most concussions was lineman (n = 3) followed by defensive backs (n = 2), and one concussion each for the positions of wide receiver, linebacker, running back, and quarterback. This observation may be due to the likelihood or force of impact per position and further research may be useful in determining why this is the case. A study by Baugh et al. has shown that, while the number of concussion doesn't seem to vary by position, the number of self-reported post-impact symptoms is highest in offensive linemen [19]. As stated above, a significant number of concussed players had a history of concussion (44%). This is not surprising, since a propensity for concussion
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in those with a history of this injury has been well documented in the literature [6,7]. This is also important to note because of possible longterm neuropsychiatric consequences currently being investigated, such as altered cognition, depression, chronic traumatic encephalopathy, and Alzheimer's disease [2,3,6,8]. In this study, there was a range of 14.6% to 110.3% increase in cumulative read time from baseline. It is known that concussions can range in severity and exhibit a variety of symptoms. This large range in the concussed players may be explained by the unique severity of each player's concussion. Future study is recommended to investigate correlation between the amount of time worsening from baseline and severity of concussion injury. In the absence of concussion, previous investigations of MMA fighters [15], rugby players [13,20,21], and college athletes [14], revealed that the KD test has “learning effects” associated with repeated testing. Galetta and colleagues hypothesized that this effect accounted for many athletes improving (decreasing) their KD times over the course of two testing sessions or between pre- and post-season measurements. While our investigation did reveal some degree of learning effect, the difference was modest compared to other studies and was not statistically significant (p = 0.73) (Table 2). This difference may be specific for younger athletes, or may be due to differences in interval between pre- and post-season testing. For instance, MMA fighters were exposed to the KD test three times in one day. In this study, time between pre- and post-season testing of concussed athletes was consistent and of substantial duration, 12 weeks, owing to the uniform high school football season in Michigan. Currently, the SCAT3 is one of the most widely utilized tools to aid in the diagnosis of concussion. In recent years ImPACT testing has been shown to also play a role in monitoring visual motor speed, reaction time, and verbal and visual memory. Each of these has been recognized as an area of impairment in concussion. The ImPACT test is the current standard used by the participating high schools for assessing concussion-related symptoms and is also utilized by the NCAA and several professional sports. It is the most widely used and validated test for assessing baseline function and return to play [1]. However, it is cumbersome in that testing requires approximately 30 min, a computer, a quiet environment, and a licensed administrator. The KD test has already been validated as a rapid sideline screening tool as discussed above [13–15]. Tjarks et al.'s study on ImPACT testing versus KD testing shows that the KD test effectively assesses recovery of oculomotor speed and visual processing which are some of the more commonly reported symptoms of concussed patients [22]. With further investigation, the KD test may gain validation as a tool for concussion detection and may be utilized in assessing a player's recovery of cognitive function, similar to the PCSS and ImPACT tests. Determining a player's return to full activity after a concussion, although still a clinical decision, has been aided by ImPACT testing. All of the high school football players in this study received baseline and post-concussion ImPACT testing in addition to King–Devick testing. It has previously been shown that the KD and ImPACT tests correlate with respect to concussion diagnosis and return to baseline function following a concussion [22]. KD performance significantly correlated with the visual motor speed/memory and reaction time components of the
Table 2 Read times.
Players with Concussion
Players without concussion
Card 1 Card 2 Card 3 Cumulative total Card 1 Card 2 Card 3 Cumulative total
Baseline tests median time in seconds (range)
Sideline tests median time in seconds (range)
Delta
p value
14.2 (10.5–18.4) 15.6 (11.4–19.2) 17.3 (11.4–19.2) 47.1 (33.3–67.5) 14.7 (9.1–26.5) 15.1 (9.7–28.9) 16.5 (9.7–41.4) 47.4 ± 9.7
22.0 (16.0–28.1) 21.2 (17.3–29.9) 24.3 (16.0–36.9) 66.2 (51.0–72.1) 14.1 (9.3–26.2) 14.9 (9.3–27.8) 16.4 (10.1–40.3) 46.8 ± 11.5
154.9% 135.9% 140.5% 140.6% 95.5% 98.7% 99.4% 98.7%
0.001 0.0008 0.004 0.003 0.50 0.31 0.80 0.73
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Table 3 Individual players with concussion.
Player 1 Player 2 Player 3 Player 4 Player 5 Player 6 Player 7 Player 8 Player 9
Baseline cumulative read time (s)
Sideline cumulative read time (s)
Sideline percent baseline (%)
Repeat (end of season) read time (s)
End of season percent baseline
42.4 44.5 58.3 35.0 47.5 59.1 43.3 47.1 54.7
65.7 51.0 89.9 73.6 92.1 90.2 56.4 54.1 66.2
155.0 114.6 154.2 210.3 193.9 152.6 130.3 114.9 121.0
42.1 43.7 61.8 60.6 60.8 58.4 42.9 NA NA
99.3% 98.2% 106.0% 173.1% 128% 98.8% 99.2% – –
NA = lost to follow-up (quit football)
ImPACT test after a concussion. This helps to demonstrate that KD may be a useful sideline screen for concussion in addition to a useful tool in monitoring recovery in the high school football player. In this study, there was circumstantial evidence that as symptoms resolved, both ImPACT scores improved and KD testing times decreased (improved). Seven of the nine concussed athletes were tested at season's end per protocol, (two of the nine concussed players were lost to follow-up). One player with residual cognitive deficit at season's end, as assessed by ImPACT testing, also had significantly slower read times on the KD test. The other re-tested players, who were cleared to play following ImPACT testing, had no residual deficit as assessed by KD testing. This suggests that, with further research, KD test may have value as a return to play test. A prior study on MMA fighters attempted to define a standardized percent increase that may define concussion using KD testing [15]. This was partly based on the fact that fighters who lost consciousness had even higher KD read times than those who suffered concussion without LOC. KD scores were also shown to correlate with PCSS and MACE scores after concussion. The authors of this paper suggested that a 5 s worsening in cumulative KD times was indicative of concussion, but this difference in time has not been further defined in other studies. In this study, the minimal increase in cumulative read time in a concussed player was 6.5 s (14%) above baseline, which fits with this hypothesis. However, no non-concussed athlete had increased (worse) post-season KD times compared to baseline, suggesting that any increase in cumulative read time was indicative of concussion in this specific cohort as indicated in the instructions for the KD test. Concussed patients exhibit a varied number of symptoms that can sometimes be difficult to diagnose at the time of injury. The KD test offers objective assessment of rapid eye movement, language, and attention that may help screen for concussion at the time of head trauma. This is significant because early diagnosis of concussion leading to removing a player from play is crucial to protecting their brain health [23]. KD testing offers the ability to efficiently and accurately screen players on the sidelines who may have suffered a concussion and quickly determine that they be removed from play until a comprehensive diagnosis can be made. Several limitations were encountered through the course of this research. First, the sample size of concussed athletes was smaller than anticipated, which creates some difficulty with respect to generalizing conclusions reached in this study. It is possible that the use of SCAT3 on field and ImPACT testing after injury to verify concussion may be a more a stringent set of criteria for diagnosis than used in other studies. Also, in the state of Michigan, there has been a dramatic increase in concussion awareness among high school athletes and their parents, coaches and medical personnel working with the sports teams. This results from educational efforts mandated by recent legislation in the state. It is possible that coaches have helped to lower concussion rates as they emphasize proper tackling and blocking techniques and players learn that “leading with your head” has health consequences. Paradoxically, this education could also lead to an under reporting of symptoms by the players as they come to realize that the diagnosis of concussion
mandates removal from play. This sentiment was expressed by a number of players during interviews for the study and has been reported previously [24]. One of the strengths of this study comes from the fact that none of the concussed players experienced vision difficulties. Kontos et al. states that vision difficulties are reported in 30% of concussed individuals [25], which may affect the sensitivity of the KD as a screening tool. This further strengthens the case for a multifaceted diagnostic process [26]. This study supports existing evidence that the KD test is effective in youth sports because it can be used by a trained layperson such as a coach, teacher, or volunteer, takes only minutes to perform, and can be administered easily at the sidelines due to its portable nature. Having such a tool is essential in contact sports where third party pressures to return to play without physician evaluation are ever-present. Future studies may show the KD test to be a useful screening tool in other youth sports and perhaps on the professional level as well. Conflicts of interest None. Acknowledgments The authors would like to thank the following individuals for their contributions: Allison Blumenthal BS, Scott Mueller BS, Collin Blattner BS, Logan McCool BS, Jacqueline Dufour BS, and Mary Predko BS. We would like to acknowledge the Medical Executive Committee at St. John Macomb-Oakland Hospital for their financial support of these research efforts. We would also like to acknowledge all of the high school football coaches and administrators who allowed us access to the athletes throughout the football season. Finally, we would like to acknowledge the athletes and their parents for their participation in this study. References [1] M. Aubry, R. Cantu, J. Dvorak, T. Graf-Baumann, K. Johnston, J. Kelly, M. Lovell, P. McCrory, W. Meeuwisse, P. Schamasch, Summary and agreement statement of the First International Conference on Concussion in Sport, Vienna 2001. Recommendations for the improvement of safety and health of athletes who may suffer concussive injuries, Br. J. Sports Med. 36 (2002) 6–10. [2] K.G. Harmon, J.A. Drezner, M. Gammons, K.M. Guskiewicz, M. Halstead, S.A. Herring, J.S. Kutcher, A. Pana, M. Putukian, W.O. Roberts, American Medical Society for Sports Medicine position statement: concussion in sport, Br. J. Sports Med. 47 (2013) 15–26. [3] N.A. Shaw, The neurophysiology of concussion, Prog. Neurobiol. 67 (2002) 281–344. [4] H.L. Laurer, F.M. Bareyre, V.M. Lee, J.Q. Trojanowski, L. Longhi, R. Hoover, K.E. Saatman, R. Raghupathi, S. Hoshino, M.S. Grady, T.K. McIntosh, Mild head injury increasing the brain's vulnerability to a second concussive impact, J. Neurosurg. 95 (2001) 859–870. [5] L. Longhi, K.E. Saatman, S. Fujimoto, R. Raghupathi, D.F. Meaney, J. Davis, B.S.A. McMillan, V. Conte, H.L. Laurer, S. Stein, N. Stocchetti, T.K. McIntosh, Temporal window of vulnerability to repetitive experimental concussive brain injury, Neurosurgery 56 (2005) 364–374. [6] N.M. Wetjen, M.A. Pichelmann, J.L. Atkinson, Second impact syndrome: concussion and second injury brain complications, J. Am. Coll. Surg. 211 (2010) 553–557. [7] C.M. Baugh, J.M. Stamm, D.O. Riley, B.E. Gavett, M.E. Shenton, A. Lin, C.J. Nowinski, R.C. Cantu, A.C. McKee, R.A. Stern, Chronic traumatic encephalopathy: neurodegeneration
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