Prediction of Post-Concussive Behavioral Changes in a Rodent Model Based on Head Rotational Acceleration Characteristics

Annals of Biomedical Engineering, May 2016

Quantifying injury tolerance for concussion is complicated by variability in the type, severity, and time course of post-injury physiological and behavioral changes. The current study outlined acute and chronic changes in behavioral metrics following rotational acceleration-induced concussion in rats. The Medical College of Wisconsin (MCW) rotational injury model independently controlled magnitude and duration of the rotational acceleration pulse. Increasing rotational acceleration magnitude produced longer recovery times, which were used in this study and our prior work as an assessment of acute injury severity. However, longer duration rotational accelerations produced changes in emotionality as measured using the elevated plus maze. Cognitive deficits were for the most part not apparent in the Morris water maze assessment, possibly due to the lower severity of rotational acceleration pulses incorporated in this study. Changes in emotionality evolved between acute and chronic assessments, in some cases increasing in severity and in others reversing polarity. These findings highlight the complexity of quantifying injury tolerance for concussion and demonstrate a need to incorporate rotational acceleration magnitude and duration in proposed injury tolerance metrics. Rotational velocity on its own was not a strong predictor of the magnitude or type of acute behavioral changes following concussion, although its combination with rotational acceleration magnitude using multivariate analysis was the strongest predictor for acute recovery time and some chronic emotional-type behavioral changes.

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Prediction of Post-Concussive Behavioral Changes in a Rodent Model Based on Head Rotational Acceleration Characteristics

Annals of Biomedical Engineering Prediction of Post-Concussive Behavioral Changes in a Rodent Model Based on Head Rotational Acceleration Characteristics MATTHEW D. BUDDE 1 2 3 4 5 ALEKSANDRA GLAVASKI-JOKSIMOVIC 1 2 3 4 5 MICHAEL MCCREA 1 2 3 4 5 SHEKAR N. KURPAD 1 2 3 4 FRANK A. PINTAR 1 2 3 4 0 Department of Pharmacology and Toxicology, Medical College of Wisconsin , Milwaukee , USA 1 Neurosurgery, Medical College of Wisconsin , Milwaukee , USA. Electronic mail: 2 Clement J. Zablocki Veterans Affairs Medical Center , Milwaukee , USA 3 acceleration , Animal model, Sports, Injury, Concussion 4 Department of Neurosurgery, Medical College of Wisconsin , Milwaukee , USA 5 Neuroscience Research Center, Medical College of Wisconsin , Milwaukee , USA -Quantifying injury tolerance for concussion is complicated by variability in the type, severity, and time course of post-injury physiological and behavioral changes. The current study outlined acute and chronic changes in behavioral metrics following rotational acceleration-induced concussion in rats. The Medical College of Wisconsin (MCW) rotational injury model independently controlled magnitude and duration of the rotational acceleration pulse. Increasing rotational acceleration magnitude produced longer recovery times, which were used in this study and our prior work as an assessment of acute injury severity. However, longer duration rotational accelerations produced changes in emotionality as measured using the elevated plus maze. Cognitive deficits were for the most part not apparent in the Morris water maze assessment, possibly due to the lower severity of rotational acceleration pulses incorporated in this study. Changes in emotionality evolved between acute and chronic assessments, in some cases increasing in severity and in others reversing polarity. These findings highlight the complexity of quantifying injury tolerance for concussion and demonstrate a need to incorporate rotational acceleration magnitude and duration in proposed injury tolerance metrics. Rotational velocity on its own was not a strong predictor of the magnitude or type of acute behavioral changes following concussion, although its combination with rotational acceleration magnitude using multivariate analysis was the strongest predictor for acute recovery time and some chronic emotional-type behavioral changes. Biomechanics; Traumatic brain injury; Angular INTRODUCTION It is becoming clear that rates of diagnosed concussion in contact sports are increasing. Comparing two studies that reported rates of concussion (per 10,000 exposures) reveals considerable increases for high school sports between the late 1990s and the 2008–2010 seasons.27,38 The comparison reveals a 94% increase in concussion rate for football, a 162% increase for women’s soccer, and a 144% increase for wrestling. Other studies have highlighted the significant increase in concussion rate in high school sports over a 6-year period, indicating that five of nine investigated sports had statistically significant increases.32 While explanations for these increases may include increased awareness about concussions by coaches, medical professionals, and athletes, increased legislation, and better reporting of concussions at the high school level, the possibility of increasing concussion incidence should not be ignored. This comes at a time of increased awareness of the chronic effects of concussions. The significant life-long effects of repetitive mild and moderate brain trauma have garnered considerable media attention. The mechanism behind these neurological declines appears to follow a dose effect phenomenon, as evidenced by boxers with neuropathological burden related to the length of a boxing career and number of bouts.9 However, even lower severity or less frequent injuries can lead to chronic difficulties. For example, the work of Guskiewicz, McCrea and colleagues has outlined significantly increased rates of chronic cognitive difficulties and emotional disturbances, including depression, for retired professional football players that had sustained 0090-6964/16/1100-3252/0 2016 The Author(s). This article is published with open access at Springerlink.com three or more concussions over the course of their career compared to players that had sustained two or fewer.16,17 The mechanism of concussion has long been associated with head impact resulting in high rate head rotational acceleration.30 Head accelerations lead to tensile and shear strains within the brain tissues that can exceed mechanical tolerance resulting in physiologic dysfunction and/or mechanical injury. The science of injury biomechanics would indicate that the onset and outcomes from concussion should then be correlated to head rotational acceleration characteristics, which could include peak magnitude, positive duration, or area under the curve (i.e., rotational velocity). In other areas of injury biomechanics, the risk of soft tissue cervical spine in (...truncated)


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Brian D. Stemper, Alok S. Shah, Rachel Chiariello, Christopher M. Olsen, Matthew D. Budde, Aleksandra Glavaski-Joksimovic, Michael McCrea, Shekar N. Kurpad, Frank A. Pintar. Prediction of Post-Concussive Behavioral Changes in a Rodent Model Based on Head Rotational Acceleration Characteristics, Annals of Biomedical Engineering, 2016, pp. 3252-3265, Volume 44, Issue 11, DOI: 10.1007/s10439-016-1647-x