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Tracking the Recovery of a Mild Traumatic Brain Injury Patient utilizing a 60-s Combined Functional Near-Infrared Spectroscopy and Psychomotor Testing Approach: A Case Study

Cory M. Smith*, Cierra B. Ugale, Matt D. Segovia, Katie M. Lee, Andrew R. Gallucci, Joshua R. Thompson, Hunter D. Dobbs, Owen F. Salmon

Robbins College of Health and Human Sciences, Human & Environmental Physiology Laboratory, Baylor University, Waco, TX USA.

*Corresponding author

*Dr. Cory M. Smith, Assistant Professor Human & Environmental Physiology Laboratory Baylor University One Bear Place #97313 Waco, Texas 76798, USA.

ABSTRACT

Identifying and tracking the recovery of patients with mild traumatic brain injuries (mTBI) has remained elusive due to the lack of non-invasive, objective neuroimaging techniques. The purpose of this case study was to provide a proof of concept for performing a combined functional near-infrared spectroscopy (fNIRS) and 60-s psychomotor vigilance testing (60-s PVT) that can identify and track the recovery of a patient with a mTBI. The patient was a 19-year-old female acrobatics and tumbling athlete who was kicked in the left temple by a teammate. Video footage of the injury was utilized to determine the region of impact and weekly fNIRS and 60-s PVT assessments were performed throughout the 10 weeks of recovery. The patient was cleared for activity based upon symptoms at week 7; however, the patient reported increased symptomology during weeks 7 and 8 following exercise. Our fNIRS neuroimaging technique was able to detect the systemic physiological responses associated with mitochondrial dysregulation and oxygen extraction fraction at weeks 1 to 8. Based on our findings, the patient remained injured at week 8, and that the physical activity performed at weeks 7 and 8 may have regressed recovery and induced additional dysfunction resulting in increased recovery time. In conclusion, we were able to identify and track the recovery of our patient with a mTBI using our non-invasive combined fNIRS and 60-s PVT approach. Results provided real time physiological responses associated with the injury throughout the recovery process.

Keywords: Mild Traumatic Brain Injury (mTBI); Functional Near-Infrared Spectroscopy (fNIRS); Recovery; Psychomotor Vigilance Test (PVT).

Introduction

Identifying and tracking the recovery of patients with mild traumatic brain injuries (mTBI) has remained elusive due to the lack of non-invasive, objective neuroimaging techniques and that each injury may be unique in its severity, signs and symptoms.1 This present case provides an overview of a novel utilization of functional near-infrared spectroscopy (fNIRS) combined with a 60-s psychomotor vigilance test (60-s PVT) for the monitoring of a patient with a severe mTBI. fNIRS examines the hemodynamic responses in brain tissue by using specific wavelength light absorbance rates to quantify the oxygenated (O2Hb), deoxygenated (HHb), and total hemoglobin (tHb) within a targeted region of the brain.2–4 mTBI’s with associated cerebral damage (e.g., cerebral hemorrhage), require increased nutrient exchange to heal causing greater blood flow to the damaged region when under load.5–8 Furthermore, following a mTBI, moderate to severe cognitive tasks are often contraindicated as they induce a worsening of symptoms.9–11 As a result, complex screening tools may induce greater severity scores immediately following a mTBI or place the patient at increased risk of adverse events such as headaches, nausea, or malaise.12,13 The 60-s PVT utilized in this case study mildly stimulates the major regions of the brain through visual, motor, and cognitive stimuli to induce a hemodynamic shift over the damaged region which would otherwise be undetectable.14,15 To our knowledge this is the longest published tracking of the recovery of a patient with an mTBI using fNIRS following injury onset.16–18 In addition, the present case is novel in that neuroimaging began within 72-hr from the onset of injury, weekly tracking was performed, and the exact time and location of injury was established through video footage of the injury’s occurrence which allowed for precise neuroimaging and tracking of the patient during their recovery.

Our fNIRS technique is ideal for real-world monitoring as it is not as impacted by movement or environmental conditions as the traditionally used electroencephalograms (EEG). In addition, fNIRS is more portable than functional magnetic resonance imagining (fMRI) techniques which are costly and cannot be performed on the field during sporting events.5,19 The fNIRS technology has been shown to have greater spatial resolution than EEG, similar to that of fMRI.2,4,20,21 In addition, fNIRS has slightly lower temporal resolution than EEG, but much greater than that of fMRI. Thus, the portability and unique blend of spatial and temporal neuroimaging resolution makes the use of fNIRS ideal for identifying and tracking mTBI in real-world environments.2,4,20,21 However, previous studies using fNIRS have shown mixed results in its ability to identify mTBI’s.17,18,22–24 We hypothesized that these conflicting results were the result of methodological approaches that included unoptimized post-processing neuroimaging data fusion and mTBI-specific analysis algorithms for regional injury determinations.17,25,26 Furthermore, other fNIRS studies have utilized O2Hb hemoglobin measures in their statistical analyses. However, many studies have reported HHb and tHb as more robust in detecting alterations in cognitive load and neuroplastic changes.3,18,27,28 Therefore, the purpose of this case study was to provide a proof of concept for performing weekly fNIRS (O2Hb, HHb, and tHb) and 60-s PVT monitoring of a unique mTBI patient suffering from severe symptoms.

Methods

Patient : The patient was a 19-year-old female acrobatics and tumbling athlete. Prior to enrollment in college, the patient had a history of concussions with prolonged recovery periods. During a synchronized tumbling pass the patient was kicked in the left temple by a teammate, followed by hitting her forehead on the mat during landing. Immediately following the impact, the patient presented with signs and symptoms (e.g., headache, altered mental status) warranting a referral to an emergency department (ED) for further evaluation. At the ED a head computerized tomography (CT) scan revealed that the patient was suffering from a severe mTBI. However, results of the CT scan did not identify a skull fracture or hemorrhaging. An assessment completed by the school’s medical staff after being released from the hospital found the patient was suffering from headaches, visual disturbances, and disorientation. Further, neurocognitive testing revealed substantial deficits in processing speed, reaction time, and executive functioning. The patient was then re-evaluated the day after the initial injury where she reported headaches, disorientation, and fatigue.

In total, the patient was symptomatic for 10 weeks following injury. Video footage of the injury was utilized to determine the region of impact and weekly neuroimaging assessments were performed throughout the 10 weeks. Recovery from the mTBI during this time was marked by a slow and steady decrease in symptoms (e.g., headaches, difficulty sleeping, sensitivity to light/noise, vision issues, dysphasia, emotional disturbances). The patient did not return to any physical activity until seven weeks after the initial injury. However, her activity was early threshold aerobic exercise primarily consisting of cycling while being monitored for increases in reported mTBI signs and symptoms. Due to the prolonged recovery and previous concussion history, the medical team and patient decided that further participation in the sport was not feasible. Thus, the patient medically disqualified from further participation. This project was approved by the institutions IRB (Approval ID#: 2012044), is aligned with the Declaration of Helsinki, and the patient’s consent was provided to publish the data within this case study. This study.29

Functional Near-Infrared Spectroscopy Signal Analysis

The overall fNIRS-derived hemodynamic responses were monitored each week for 10 weeks of the patient’s recovery beginning after the onset of the injury. The location of placement for the fNIRS sensors were determined based on video footage of the injury and athletic trainers present at the time of injury. fNIRS hemodynamic monitoring were collected over left (Injured) and right (Control) superior temporal region of the patients’ head using a 4x1 optode to receiver layout which was secured to the head with a full head neoprene cap, chin strap, and pressure relief system to maintain sensor placement (Figure 1) (OxyMon MKII, Artinis Medical Systems, Einstinweg, Netherlands). The centerpoint of the 4x1 sensor grid was the location of impact and the identical location on the opposing side of the head. Each of the 4 optodes on each region of the head were sampled at 10 Hz for each of the 762 and 848 nm wavelengths utilized to monitor the hemodynamic responses. Each wavelength penetrates through the skull and into the cerebral cortex at a distance of ~2.5 cm (Figure 2). The thickness of the skull was estimated based on the patients age and utilized to calculate a correction factor for the differential path-length factor (DPF) caused by the refraction of the skull (Equation 1; Figure 2). 4,30 A first order processing of the fNIRS signals were performed by filtering for Mayer waves, respiration, and heart pulsation by examining the power density spectrum prior to the continuous wavelet (CWT) analysis (Equation 2 and 3). A Morlet Wavelet was utilized for the CWT transform using time-step coefficients without any overlap was then performed. The Wavelet coefficients were determined from the culmination of all the CWT data over each weeks 60-s PVT test and was used to further analyze the CWT Multiscale Peak Detection to quantify the amplitude of each CWT (Equation 4). This analysis allowed for the calculation of fNIRSamp values for O2Hbamp, HHbamp, and tHbamp. Together, these metrics provide the regional cerebral blood flow (tHbamp), metabolic stress (HHbamp), and available oxygen (O2Hbamp) in the Control and Injured regions of the brain. Each hemisphere’s 4 optode grid channels were then summated to provide an individual activation level for each locations site of interest during each week’s 60-s PVT (Equation 4).

Equation (1)  DPF=4.99+0.067(Age Years0.814)

Equation 1 is used for calculating the age-corrected DPF that is entered into Equation 2, the modified Lambert-Beer law, that corrects for the effects of altered light scattering and paths during the near-infrared spectroscopy measurement.

Equation (2) ∆C=∆ODλ/(ελ*L*DPF)

Equation 2 is the modified Lambert-Beer law equation used for determining concentrations from each of the wavelengths. OD = optical density, ελ = chromophore’s extinction coefficient, λ = wavelength, C = concentration, L = optode to receiver distance.

Figure 1: Functional Near-Infrared Spectroscopy (fNIRS) setup for the impacted and unimpacted region of the head in the patient. This displays the 4 optode and receiver placements 4 x 1 grid approach utilized in this study. The optodes cycled 2 wavelengths of light, each at 10Hz to be detected with the receiver located in the center of the 4x1 cluster.

Equation (3) μa (λ)-εH2O (λ) cH2O=εO2Hb (λ)cO2Hb+εHHbHHb (λ)cHHb

Equation 3 is involved in the 1st order processing and corrects for the water content within the signal absorption rates. ε = extinction coefficient, λ = wavelength, c = concentration

Equation (4)

Equation 4 provides the individual channel calculation in each prefrontal cortex hemisphere Morlet wavelet analysis. The CWT transform will be utilized with a 20 scale and 512 time-step coefficients without any overlap. The Wavelet coefficients were determined from the culmination of all the CWT data over each individual epoch to determine the Morlet CWT frequency of the signal. The data from the Morlet Wavelet was further analyzed with CWT Multiscale Peak Detection to quantify the amplitude of each channel, hemisphere, and timepoint. This analysis will allow for the calculation of fNIRSamp values for O2Hb, HHb. And tHb. Each hemispheres 4 optode grid channels relative measurements was then summated to provide an singular value for each hemisphere averaged across the 60-s PVT for each of the 10 weeks.

Three exploratory t-tests were performed on the mean Control and Injured tHbamp, HHbamp, and O2Hbamp measures, collapsed across the 10 weeks for sufficient data points, to determine the gross differences in hemodynamics throughout the 60-s PVT.

Psychomotor Vigilance Test

A 60-s PVT was performed each week while wearing the fNIRS neuroimaging sensor on the injured and control regions of the patient’s brain. The 60-s PVT test was performed on a touch screen tablet (iPad 10.2in 9th generation, Apple, Cupertino, CA) using the Research Buddies software (Research Buddies Version 1.53). During each visit, the patients’ index finger on the dominant hand was placed on the lower corner of the tablet. The researcher then started the 60-s PVT, and the patient would tap the center of the screen as quickly as possible when a number appeared. Upon completion of the 60-s PVT, the average, fastest, and slowest reaction time were recorded (Figure 3).

Figure 2: Visualization of the fundamental principles underlying functional near-infrared spectroscopy (fNIRS) for cerebral hemodynamics from the perspective of one of the 4 optodes utilized in each 4x1 grid.

Figure 3: Results of the 60-s Psychomotor Vigilance Reaction Time test including the average, fastest, and slowest reaction time for each weekly visit during the 10-wk recovery period. The dashed line represents the average reaction time captured within 72-hr of injury.

Figure 4: The continuous wavelet analysis (CWT) amplitudes averaged across all 4 optode in the 4x1 grid and averaged across the 60-s psychomotor vigilance test during each of the 10 weeks. The square reflects the Injured region of the temples cerebral cortex and the circle reflects the Control (uninjured opposing temple location of the cerebral cortex) for the fNIRS derived a) total hemoglobin responses (tHb); b) oxygenated hemoglobin response (O2Hb); and c) deoxygenated hemoglobin response (HHb). The dashed line represents the neuroimaging amplitude value measured within 72-hr from the Injured side of the brain while the dotted line represents the same timepoint for the Control region of the brain.

Results

Figure 3 displays the weekly results from the 60-s PVT which indicated that the average 60-s PVT (PVTAVG) reaction time improved by Δ28%, the fastest 60-s PVT (PVTF) reaction time speed increased by Δ 36% while the slowest 60-s PVT (PVTS) reaction had a Δ18% improvement (Figure 3).

For the fNIRS CWT amplitude neuroimaging measurements, there were negligible changes to the control region of the brain for tHb CWT amplitude (tHbamp; Δ6%), HHb CWT amplitude (HHbamp; Δ6%), or O2Hb CWT amplitude (O2Hbamp; Δ8%) (Figure 4a, 4b, 4c). Unlike the control region, the injured region of the brain tracked large improvements in tHbamp (Δ60%), HHbamp (Δ 35%), and O2Hbamp (Δ63%) (Figure 4a, 4b, 4c).

Figure 5 displays the wavelet heatmap visual results from a single 60-s PVT tHb broken down into 6 separate 10-s epochs to display the impact a 60-s PVT has on improving the identification of an mTBI utilizing the fNIRS approach in this patient (Figure 5).

Th exploratory t-tests indicated that there was a significant difference between Control and Injured regions of the brains tHbamp (Control: 102 ± 7.4 CWTamp, Injured: 159 ± 44.0 CWTamp; p < 0.001), HHbamp (Control: 102.6 ± 4.7 CWTamp, Injured: 142 ± 23.1 CWTamp; p < 0.001), and O2Hbamp (Control: 100 ± 4.9 CWTamp, Injured: 152 ± 42.3 CWTamp; p = 0.001).

Discussion

Psychomotor Vigilance Testing

The 60-s PVT tracked improvements in the patients’ symptoms with a 16% decrease in average reaction time from week 1 to week 7 and a 40% decrease from week 1 to week 10 (Figure 3). The patient was cleared for return to activity at week 7, which corresponded to the quickest of the first 7 weeks post-injury 60-s PVT results. These findings were aligned with Sinclair et al., 2013 who reported average PVT times above 400-ms in >90% of TBI patients and  average PVT times less than 400-ms in >95% of non-TBI patients.14 Based on these findings, the 60-s PVT results of our patient suggested an impairment due to the mTBI (710-ms) and that the 60-s PVT was capable of tracking general improvements throughout the recovery process (710 to 509-ms) which aligned with the return to play decision. It is unclear, however, how closely the 60-s PVT alone is able to quantify injury severity as it has been suggested that a PVT has difficultly determining differences in patient injury severity scores.14 In a previous study31 that examined healthy, military non-TBI patients suffering from extreme hypoxemia and physical fatigue reported an average 60-s PVT time ranging from 380-450-ms. Taken together, the findings of these previous studies suggest that a 60-s PVT can help to identify deficits and potentially severity, but the 60-s PVT alone is unable determine if an mTBI occurred and its injury severity. However, the addition of our fNIRS neuroimaging technique coupled with the 60-s PVT results may allow for a methodology of tracking the occurrence and severity of mTBI patients.

Figure 5: Heat map visual display of the 4x1 sensor grid wavelet for total hemoglobin hemodynamic response over the Control (unimpacted) and Injured (Impacted) regions of the patients head. The hand-eye coordination and motor control required to successfully perform the psychomotor vigilance test displays its ability to elicit greater detectable changes in the hemodynamic responses over the injured region.

functional Near-Infrared Spectroscopy: Neuroimaging: Neuroimaging the contralateral side of the brain as a Control was effective for identifying the hemodynamic and metabolic differences from the Injured region of the brain in our patient as a pre-injury image was unavailable. The relatively consistent tHbamp, HHbamp, and O2Hbamp metrics across the 10 weeks for the Control compared to the Injured side reflects a low neurophysiological load placed on the Control region of the brain typical of a non-mTBI patient during the 60-s PVT (Figure 4).2,26 Furthermore, Figure 5 illustrates the similarities in the neurophysiological load placed on the Control and Injured regions of the brain at the initial 0 to 10-s of the 60-s PVT, however, after 30-s of load a greater hemodynamic and metabolic responses occurred in the Injured but not the Control region of the brain. Thus, the 60-s PVT load placed on the brain was minimal enough to not impact the Control region of the brain while sufficient at stimulating a response from the Injured region of the brain. Therefore, the utilization of a Control region was effective and allowed us to develop a target recovery threshold for the Injured region of the brain to match the tHbamp, HHbamp, and O2Hbamp of the Control region.

The combined tHbamp, HHbamp, and O2Hbamp pattern of responses throughout the 10 weeks of recovery indicated maintenance of the patients Oxygen Extraction Fraction (OEF) in the Injured region of the brain. 32 The HHbamp and O2Hbamp ratio remained relatively constant in the Injured region of the brain with a concomitant increase in tHbamp which suggested that greater oxygenation utilization was required in the Injured region of the brain compared to the Control (Figure 4). The overall increased blood flow to the Injured region and increased metabolic demand, as indicated by the greater HHbamp, likely aimed to offset the mTBI associated Ca2+ overload within the patient. Increasing of the patients overall regional blood flow (tHbamp) to the Injured region may reflect a protective mechanism to avoid the catabolic effects of a Ca2+-induced intracellular dysregulation that has been shown to result in the overproduction of free radicals, activation of cell death signaling pathways and stimulation of inflammatory responses.33–35 That is, the fNIRS responses captured throughout the recovery of this patient tracked with the expected systemic physiological responses associated with the maintenance of OEF. Furthermore, it has been well established that mTBI’s result in mitochondrial dysregulation which result in a greater hemodynamic shift to the injured region of the brain to provide sufficient oxygen, dilution, and clearance rates for the metabolic byproducts.33,34 It is hypothesized that the combined mitochondrial dysregulation induced hemodynamic shift was likely the driving factor for the increased metabolic stress (HHbamp) while OEF further stimulated a greater hemodynamic flow to the Injured region of the brain to avoid further injury associated with a buildup of metabolic byproducts. The combined regional cerebral blood flow regulation pattern (tHbamp) and increased metabolic demand captured in this patient indicated that the damage to the patient’s brain was detectable using our fNIRS approach. Furthermore, the combined utilization of our CWT tHbamp, HHbamp, and O2Hbamp methodology allowed for identification of the hemodynamic shifts associated with the injury and increased load induced by the 60-s PVT.

In our patient, all fNIRS metrics that were elevated from weeks 1 to 8 improved to within Control values at week 9 and remained at the Control levels at week 10 (Figure 4). The tracked improvements in all fNIRS measures suggest that this patient’s recovery became physiologically improved at week 9, however, the patient reported minimal symptomology at rest at week 7 which cleared the patient to begin light physical activity. During weeks 7 and 8 the patient reported increased symptomology when exercising which was her rate limiter to perform physical activity. Considering the onset of the symptomology due to exercise and the fNIRS detected hemodynamic shifts associated with mitochondrial dysregulation coupled with OEF, the patient may have been less symptomatic if exercise was resumed at week 9.32,34 Specifically, the improved fNIRS and 60-s PVT metrics at week 9 were closely aligned with the Control and expected reaction time values, respectively, suggesting that our fNIRS approach could track the physiological recovery in this patient (Figure 4). Early physical activity in patients with mTBI’s has been linked to increase metabolic byproduct accumulation, greater hemodynamic shifts, potential reduced recovery rates, and increased symptomology.32,34,36,37 Thus, the elevated tHbamp, HHbamp, and OxyHbamp values at week 8 suggest that the physical activity performed at weeks 7 and 8 may have regressed recovery and induced additional dysfunction, lengthening recovery time. Therefore, further development of this non-invasive neuroimaging approach will provide clinicians with a useful assessment tool to make more informed decisions on the rate of recovery and activity a patient may be prescribed.

Limitations: This was an exploratory case study performed on a single patient to examine the clinical feasibility of the fNIRS and 60-s PVT analysis approach which will need greater refinement and development prior to clinical adoption. We acknowledge that greater data from a larger population should be studied to make this technology useable when real-time accounts or video footage of the injury site is unavailable. Thus, data from this study should not be applied to a broader patient pool until further studies focusing on the refinement and application of this approach is completed. The data from this case study does provide the foundational information needed to replicate the study methodology and highlights the relevance to the clinical community aiming to develop non-invasive mTBI monitoring devices.

Conclusion

In conclusion, the 60-s PVT was capable of detecting deficits in our patient, however, the 60-s PVT alone was unable to determine injury severity. The addition of our fNIRS neuroimaging technique was able to detect the systemic physiological responses over the injured region of the brain that align with mitochondrial dysregulation induced hemodynamic shifts and increased metabolic stress (HHbamp). In addition, tHbamp and HHbamp identified OEF which further stimulated a greater hemodynamic flow to the Injured region of the brain to avoid a buildup of metabolic byproducts. The neuroimaging from the contralateral side of the brain was effective as a Control in our patient as a pre-injury image was unavailable. Using the Injured and Control region neuroimaging, we determined the elevated tHbamp, HHbamp, and OxyHbamp values at week 8 suggest that the physical activity performed at weeks 7 and 8 may have regressed recovery and induced additional dysfunction, lengthening recovery time. Therefore, this case study showed that a combined 60-s fNIRS neuroimaging and PVT technique was capable of detecting the patients mTBI and tracked her recovery better than subjective assessments. Furthermore, the physiological data obtained through our non-invasive neuroimaging approach was able to identify the patient’s physiological response including potential mitochondrial dysregulation and OEF. Therefore, the physiological responses and recovery state capture in our patient indicates that the weekly assessments of a combined 60-s fNIRS and PVT approach could provide clinically relevant data on the recovery status and injury severity. Future research should focus on the development of fNIRS threshold values that can be utilized to better identify the severity of a mTBI and its associated physiological responses in a large sample of mTBI patients.

Acknowledgements: We would like to thank the patient for their time and willingness to volunteer for this study. In addition, we would like to thank Baylor Athletics Executive Senior Associate Athletic Director Kenny Boyd, Associate Athletic Director Carrie Rubertino Shearer, and all the athletic trainers who assisted in this project.

Funding: The authors declare that no funds, grants, or other support were received during the preparation of this manuscript. Competing Interests: On behalf of all authors, the corresponding author states that there is no conflict of interest.

Author Contributions: CMS: Study design, advisement, and the first draft of the case study report; CBU: Material preparation, case study report, data collection, interpretation, and analysis; JRT, HDD, MDS, and OFS: Data 7 Copyright © *Cory M. Smith Citation: *Cory M. Smith. Tracking the Recovery of a Mild Traumatic Brain Injury Patient utilizing a 60-s Combined Functional Near-Infrared Spectroscopy and Psychomotor Testing Approach: A Case Study. Jour of Clin Cas Rep, Med Imag and Heal Sci 7(1)-2024. DOI: 10.55920/JCRMHS.2024.07.001279 collection, interpretation, and analysis; ARG and KML: Study design, manuscript preparation, and clinical oversight. All authors assisted with writing and editing versions of the final report.
Ethics Approval: This project was approved by the institution IRB (Approval ID#: 2012044), is aligned with the Declaration of Helsinki, in compliance with ethical standards.

Consent to participate: An IRB informed consent was obtained by the participant prior to participation and the individual was made aware of data collection to be utilized for this case study report.

Consent to publish: The participant has consented to the submission of the case report to the journal.

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Journal of Clinical Case Reports, Medical Images and Health Sciences (ISSN 2832-1286) is a peer-reviewed journal dedicated to publishing clinical images from all sectors of medicine. The goal of this magazine is to disseminate information about new discoveries and treatments in science and medicine.

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