Name: objectively assessing sports concussion utilizing visual evoked potentials
Uploaded: 2021-04-27T14:00:00
Duration: 12 min 11 s
Description: Watch this Scientific Journal Video about Objectively Assessing Sports Concussion Utilizing Visual Evoked Potentials at JoVE.com

The equipment utilized in the initial experiment (investigative SSVEP) was provided by the School of Aerospace, Mechanical and Mechatronic Engineering at The University of Sydney. Equipment utilized in the latter half of the study, the integrated SSVEP and EEG systems, were provided by HeadsafeIP.

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The authors declare potential conflicts of interest and state them below:
Adrian Cohen is a director of HeadsafeIP Pty Ltd and is noted on Patent applications related to technology in this area.
Dylan Mahony is an employee of HeadsafeIP. HeadsafeIP undertakes research, development, and commercialization of concussion-related technologies. HeadsafeIP Pty. Ltd may benefit financially if products related to this research are successfully marketed.
Daryl Fong is an employee of Cryptych Pty Ltd. Cryptych Pty Ltd provides consulting services to HeadsafeIP on the compliant manufacturing of its device with respect to regulatory requirements.
David Putrino, Joseph Herrera, and Rebecca Baron are employees of the Icahn School of Medicine at Mount Sinai and participate in sponsored research investigating the use-cases of the improved SSVEP device.

This is the first study to develop a protocol that identifies differences in SSVEP responses in healthy male amateur ruby union players at the three stages of a concussion; pre-injury (baseline), concussed, and recovered (Figure 1). The method included the recruitment and screening of 65 participants who were routinely assessed with an investigational SSVEP setup over the course of a competitive season. As the SSVEP setup was relatively simple and portable, all assessments were conducted in a non-clinical environment, demonstrating the potential use as a point-of-care concussion assessment. The study successfully demonstrated that an individual's ability to generate SSVEPs is attenuated following a diagnosed concussion. The depressive impact of a concussion was seen to diminish following a defined recovery period, as seen when SSVEP values returned to a pre-concussed level for each individual. Statistical analysis between the participant groups showed a significance in the SSVEP attenuation effects. The high test-retest reliability in non-concussed participants highlighted the stability of the electrophysiological biomarker in simple and more refined portable SSVEP systems (Table 2). Additionally, the absolute agreement between an SSVEP system and a traditional EEG amplifier, validates the technology for use as a medical aid capable of obtaining research quality EEG signals (Figure 10).
Since this study was dependent on participants volunteering for post-injury as well as repeated assessments during the rugby season, some logistical modifications had to be made to the method. The estimated time periods between baseline and retests had to be flexible to accommodate the participant's schedules. Despite these measures, some players were still lost to follow up for a variety of miscellaneous reasons, including non-related injuries or lack of interest. This resulted in the use of a more comprehensive statistical calculation, ICC, for the device's reliability across weeks. No adverse events to the SSVEP setup were observed. Some logistic issues were encountered that required minor modifications of the protocol: long or thick hair in particular proved troublesome in acquiring good contact between the headset and the participant's scalp. As poor contact would decrease the quality of the EEG readings (Figure 4), participants with long or thick hair were required to brush and hold their hair up and out to the side of their head while the sensors were placed. An additional exclusion criterion was generated due to this issue, where individuals with complex hairstyles (e.g., dreadlocks) were excluded from this study.
As previously outlined in this paper, current concussion assessment tools are highly subjective and are at the risk of manipulation by an athlete that can ultimately hinder a clinician's ability to make a crucially important diagnosis34. Some athlete tracking studies have attempted to investigate a more objective biomarker for concussion through the use of radiological modalities such as magnetic resonance imaging (MRI) and computed tomography (CT). However, these methods only provide information about macroscopic structural injuries such as hemorrhages which vary from the definition of concussion as a functional brain injury6,35. The results of this study are supported by previous studies that demonstrated VEP to be a functional biomarker36, which is attenuated or delayed in the presence of concussion21,37,38. While there are similarities in these previous VEP study methods with respect to our physical setup and hypothesis, our study expands on the literature via the use of SSVEP over VEP. Furthermore, the protocol varies by investigating real-time assessments of players at the three stages of a concussion compared to traditional control vs concussed case studies. Additionally, the method extends its investigative power by comparing innovative and traditional EEG systems to distinguish potential dissimilarities that may limit their accuracy in obtaining objective electrophysiological measurements. Thus, the protocol used in this study provides a unique and valuable addition to existing literature on objective concussion biomarkers.
Despite the overall success of this protocol, there are several limitations to note. For example, a small degree of intra-participant variability in background EEG noise for assessment conducted in immediate succession was noted. Two protocol-design limitations may prove at fault for this first variability: the first being the 14-channel EEG system's lack of high-fidelity impedance feedback and loose constraints for the effects of fatigue and environmental influence on the subject's attentiveness. While this intra-participant variability was not seen with the other EEG systems used in this protocol, it is worth exploring these effects in more detail to confirm their cause is a result of the headset's design and not an unidentified natural occurrence. Second, most participants had larger SSVEP signals after the second assessment versus the first (Table 1). This may be the result of participants becoming more familiar with the assessment process and consequent behavioral adaptations to the equipment setup, including reduced blinking and restlessness during repeat stimulus presentation. Further studies are needed to determine whether there is indeed a familiarization effect to the SSVEP protocol and, if so, what potential modifications need to be made to reduce its occurrence in future studies. Lastly, it is important to note that due to the extensive dependence on volunteers from a relatively small population of individuals (those at high risk of concussion occurrence with the willingness to be repeatably examined), this study was limited to a small sample size of 65 participants, 12 of whom suffered a concussion. Studies with a larger cohort size will be needed in order to evaluate the robustness of this protocol's assessment of concussion, particularly its sensitivity and specificity. It would also be interesting to see this protocol replicated in a range of age groups whose brain development states vary, from those still developing (adolescents) to those with potential cognitive decline (elderly) and delineate whether or not responsivity significantly differs. With respect to the improved SSVEP system, its comparative study highlighted the in-built limitations of the device in comparison to traditional EEG systems. Traditional EEG systems generally adopt the full 10-20 system of montages, which comprise 21 electrode sites (Figure 7B). The SSVEP system on the other hand only uses three electrode channels (O1, O2, and Oz) corresponding to the visual cortex (Figure 7A). This reduction in capability means the system has a narrower scope of EEG applications and limits the potential analysis that can be conducted on the electrophysiological data obtained within this protocol.
As previously mentioned, further research is required to overcome the limitations of this protocol and test its strength on a larger cohort to assess whether its outcomes are able to be generalized. More importantly, additional studies are required to better understand the mechanisms underlying our finding in SSVEP attenuation. For instance, the changes in SSVEP response found in our concussed participants are most likely representations of disturbances in neuronal function, but it is not yet established whether these are primary (e.g., damaged white matter) or secondary (e.g., neuroinflammatory) phenomena. One potential future application of this method is the investigation into the recovery period associated with neuronal depression and concussion individualized to the subject. A deeper insight into this recovery period may see amendments made to sports return to play (RTP) rules and regulations that better protect an injured athlete. This method also introduces the practicality of a portable SSVEP system applied in non-clinical settings, such as a concussion assessment delivered expediently on the sideline of a sporting field. This has the potential to provide significant benefit to not only medical professionals, but coaches, athletes, and their respective families to address the negative physiological effects of concussion and Second Impact Syndrome10,11. The generation of improved SSVEP systems, such as the portable SSVEP system utilized in this study, may see more advanced equipment and technological applications arise in the field of neurophysiology and SRC that will prove beneficial for the success of future studies.
In summary, this protocol proved successful in its aim of identifying SSVEP as an objective biomarker for concussion in contact sport athletes. The study as a whole provides evidence that SSVEP are significantly attenuated in the presence of a concussion and are capable of being reliably produced at a research quality level through a simplified portable EEG system. We, therefore, propose that SSVEP may be used as a supplemental aid for the assessment of concussive injuries, in particular, the sideline assessment of SRC. Further studies with more refined protocols, advanced techniques, and improved equipment may build upon this study and provide critical information to combat the detrimental effects of concussions on athletes' lives.

People now-a-days are greatly aware of the morbidity caused by brain injuries in sport1. A sports related concussion (SRC) is a form of mild traumatic brain injury (mTBI) that is frequently reported in contact sports such as football, rugby, and boxing2,3,4. The biomechanical transduction of impulsive force to the brain following an impact on the field results in a disruption of neuronal function, leading to both immediate and transient symptoms that affect an athlete&#39;s physical, cognitive, and emotional state1,5. In most cases, these symptoms subdue within a short period of time, granted the athlete is appropriately treated and not exposed to further impacts6.
As SRC is detrimental to the neurological health of players, sports&#39; governing bodies face the challenge of employing accurate and timely concussion diagnosis to allow for a safe return-to-play protocol5,7,8,9. However, concussion detection can be precluded by athletes who minimize or deny symptoms to avoid a concussion diagnosis, thus accelerating their return to play. These actions can potentially increase their risk of Second Impact Syndrome, a condition in which rapid cerebral edema forms following a second head injury during the concussion recovery phase10. Additionally, due to the lack of education around concussion diagnosis and the variable nature of its physiological definition, it is not uncommon for SRC to go unreported or misdiagnosed11. Unfortunately, long periods of repeated and inappropriately managed concussions may lead to a range of chronic neurological impairments, such as chronic traumatic encephalopathy (CTE), which is strongly associated with SRC12,13,14.
In an effort to combat the challenges associated with SRC, sports organizations utilize a variety of concussion assessment tools. The most commonly used and accessible tool, sports concussion assessment tool (SCAT), is a standardized paper test that incorporates physical and cognitive assessments in combination with scaled symptom reporting15,16. However, previous studies have demonstrated that symptom reporting is subjective and unreliable by identifying gender differences within mTBI groups and outliers in the control group17,18. More advanced tools that are utilized at a professional level, such as the Immediate Post-Concussion Assessment Tool (ImPACT), which operates as a Computerized Neurocognitive Test (CNT), also fall victim to manipulation as they require active participation and effort from the athlete. Despite built-in checks for manipulation in CNTs, research has shown that they are prone to ceiling effects and suffer poor reliability19,20. The limitations of these existing assessment tools in combination with a more public understanding of the significant health effects of SRC have resulted in a critical need for an objective biomarker that can accurately and timely diagnose a concussion.
One field that has shown promise in identifying an objective biomarker for concussion is electrophysiology. There is emerging evidence that event-related potentials, in particular visual evoked potentials (VEP) are impaired following a concussion21,22. One subset of VEP; steady-state visual-evoked potentials (SSVEP) are an objective, quantifiable fluctuation of electrical activity that occurs in the brain in response to a specific set of visual stimuli, as measured by electroencephalogram (EEG) technology23,24. SSVEP offer an improved resistance to noise artifacts and variable contact impedance to conventional VEP measurements. Also, due to the controlled frequency of the visual stimulus, there is a reduction in synchronicity between EEG recordings and stimulus, resulting in a more simplified electrical model25,26. This approach has been validated with frequencies between the 12-15 Hz range producing an optimal response of salience for flicker type stimuli27. Overall, these advantages mean SSVEP offer a more robust electrophysiological measurement that can be used in a non-clinical setting such as sports fields and physician offices. This sideline application possibility in combination with the technology&#39;s positive results in previous literature makes it a promising candidate for the identification of an objective biomarker for SRC.
The goal of this study was to investigate potential differences in SSVEP that were recorded from athletes who were assessed by an experienced sports doctor as healthy, concussed, or recovered from a recent concussion. The methodology of the study entailed 65 male amateur rugby union players being routinely assessed with a portable SSVEP system over an 18-week competitive season. Players are to be assessed for a baseline prior to the commencement of full-contact training and re-assessed within 72 h following competitive games. Players who were injured during the season were evaluated for concussions by the team&#39;s physician and re-assessed with the SSVEP system for post-injury and recovery readings. Additionally, this study extends its protocol to validate portable SSVEP system&#39;s ability to obtain research-quality EEG readings that can potentially aid in the sideline assessment of SRC.

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			<td>Ag-AgCl Electrodes</td>
			<td>Compumedics</td>
			<td>97000153</td>
			<td>Disposable EEG electrode Wires</td>
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		<tr>
			<td>Cardboard VR</td>
			<td>Google</td>
			<td>87002823-01</td>
			<td>VR Frame</td>
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			<td>CaviWipes</td>
			<td>Metrex</td>
			<td>13-1100</td>
			<td>Disinfectant Wipes</td>
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			<td>Emotiv Xavier</td>
			<td>Emotiv</td>
			<td>EMO-BCI-ONET-MAC-01</td>
			<td>EEG Headset Software / Contact Quality</td>
		</tr>
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			<td>EPOC Felt Sensors</td>
			<td>Emotiv</td>
			<td>EMO-EPO-FELT-00</td>
			<td>EEG soft electrode contacts</td>
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			<td>USB Reciever Universal Model</td>
			<td>Emotiv</td>
			<td>EMO-EPO-USB-04</td>
			<td>Signal Reciever for 14 channel EEG Headset</td>
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			<td>EPOC+</td>
			<td>Emotiv</td>
			<td>EPOC+ V1.1A</td>
			<td>14 Channel EEG headset</td>
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			<td>Excel 2016</td>
			<td>Microsoft</td>
			<td>KB4484437</td>
			<td>Spreadsheet Software</td>
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			<td>Grael 4K EEG Amplifier</td>
			<td>Compumedics</td>
			<td>928-0002-02</td>
			<td>Clinical EEG / 40 Channel EEG Amplifier Unit</td>
		</tr>
		<tr>
			<td>iPad 5th Generation</td>
			<td>Apple</td>
			<td>A1822</td>
			<td>iOS Device</td>
		</tr>
		<tr>
			<td>iPhone 6s</td>
			<td>Apple</td>
			<td>A1633</td>
			<td>iOS Device</td>
		</tr>
		<tr>
			<td>iTunes</td>
			<td>Apple</td>
			<td>V12.5.5.5</td>
			<td>Mobile Device Management Utility</td>
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		<tr>
			<td>MATLAB</td>
			<td>MathWorks</td>
			<td>&#160;R2015b</td>
			<td>Numerical Computing Software</td>
		</tr>
		<tr>
			<td>Nurochek iOS App</td>
			<td>HeadsafeIP</td>
			<td>HS02</td>
			<td>SSVEP iOS App Software</td>
		</tr>
		<tr>
			<td>Nurochek System</td>
			<td>HeadsafeIP</td>
			<td>HS01</td>
			<td>Portable SSVEP System</td>
		</tr>
		<tr>
			<td>Polyurethane Sensor Cylinders</td>
			<td>Headsafe</td>
			<td>HSIP01-213</td>
			<td>EEG soft electrode contacts</td>
		</tr>
		<tr>
			<td>Profusion EEG 5</td>
			<td>Compumedics</td>
			<td>AH744-00</td>
			<td>Clinical Neurology Software for EEG Amplifier</td>
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		<tr>
			<td>Quik-Gel Electrolyte</td>
			<td>Compumedics</td>
			<td>92000016</td>
			<td>EEG Conductive Gel</td>
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			<td>Renu Fresh Solution</td>
			<td>Bausch+Lomb</td>
			<td>435720</td>
			<td>Saline Solution</td>
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			<td>SPSS 24</td>
			<td>IBM</td>
			<td>CRZ0WML</td>
			<td>Statistical Analytics Software</td>
		</tr>
		<tr>
			<td>Ten20 Paste</td>
			<td>Weaver</td>
			<td>92100031</td>
			<td>EEG Skin Prep Gel/Paste</td>
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		<tr>
			<td>Vaio Pro 11</td>
			<td>Sony</td>
			<td>SVP1132A1CL</td>
			<td>Computer / Laptop</td>
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			<td>Xperia Z1</td>
			<td>Sony</td>
			<td>C6906</td>
			<td>LCD Smartphone</td>
		</tr>
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objectively assessing sports concussion utilizing visual evoked potentials

A portable system capable of measuring steady-state visual-evoked potentials (SSVEP) was developed to provide an objective, quantifiable method of electroencephalogram (EEG) testing following a traumatic event. In this study, the portable system was used on 65 healthy rugby players throughout a season to determine whether SSVEP are a reliable electrophysiological biomarker for concussion. Preceding the competition season, all players underwent a baseline SSVEP assessment. During the season, players were re-tested within 72 h of a match for either test-retest reliability or post-injury assessment. In the case of a medically diagnosed concussion, players were reassessed again once deemed recovered by a physician. The SSVEP system consisted of a smartphone housed in a VR-frame delivering a 15 Hz flicker stimulus, while a wireless EEG headset recorded occipital activity. Players were instructed to stare at the screen's fixation point while remaining seated and quiet. Electrodes were arranged according to the 10-20 EEG-positioning nomenclature, with O1-O2 being the recording channels while P1-P2 the references and bias, respectively. All EEG data was processed using a Butterworth bandpass filter, Fourier transformation, and normalization to convert data for frequency analysis. Players SSVEP responses were quantified into a signal-to-noise ratio (SNR), with 15 Hz being the desired signal, and summarized into respective study groups for comparison. Concussed players were seen to have a significantly lower SNR compared to their baseline; however, post-recovery, their SNR was not significantly different from the baseline. Test-retest indicated high device reliability for the portable system. An improved portable SSVEP system was also validated against an established EEG amplifier to ensure the investigative design is capable of obtaining research quality EEG measurements. This is the first study to identify differences in SSVEP responses in amateur athletes following a concussion and indicates the potential for SSVEP as an aid in concussion assessment and management.

Watch this Scientific Journal Video about Objectively Assessing Sports Concussion Utilizing Visual Evoked Potentials at JoVE.com

Objectively Assessing Sports Concussion Utilizing Visual Evoked Potentials

A portable system capable of measuring steady-state visual-evoked potentials was developed and trialed on 65 amateur rugby players over 18 weeks to investigate SSVEP as a potential electrophysiological biomarker for concussion. Players' baselines were measured pre-season, with retesting for reliability, concussion, and recovery assessment being conducted within controlled time-periods, respectively.

A portable system capable of measuring steady-state visual-evoked potentials (SSVEP) was developed to provide an objective, quantifiable method of ...

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