Mild Jugular Compression Collar Ameliorated Changes in Brain Activation of Working Memory after One Soccer Season in Female High School Athletes

Abstract

Recent neuroimaging studies have suggested that repetitive subconcussive head impacts, even after only one sport season, may lead to pre- to post-season structural and functional alterations in male high school football athletes. However, data on female athletes are limited. In the current investigation, we aimed to (1) assess the longitudinal pre- to post-season changes in functional MRI (fMRI) of working memory and working memory performance, (2) quantify the association between the pre- to post-season change in fMRI of working memory and the exposure to head impact and working memory performance, and (3) assess whether wearing a neck collar designed to reduce intracranial slosh via mild compression of the jugular veins can ameliorate the changes in fMRI brain activation observed in the female high school athletes who did not wear collars after a full soccer season. A total of 48 female high school soccer athletes (age range: 14.00-17.97 years) were included in the study. These athletes were assigned to the non-collar group (n = 21) or to the collar group (n = 27). All athletes undewent MRI at both pre-season and post-season. In each session, a fMRI verbal N-Back task was used to engage working memory. A significant pre- to post-season increase in fMRI blood oxygen level dependent (BOLD) signal was demonstrated when performing the N-back working memory task in the non-collar group but not in the collar group, despite the comparable exposure to head impacts during the season between the two groups. The collar group demonstrated significantly smaller pre- to post-season change in fMRI BOLD signal than the non-collar group, suggesting a potential protective effect from the collar device. Significant correlations were also found between the pre- to post-season increase in fMRI brain activation and the decrease in task accuracy in the non-collar group, indicating an association between the compensatory mechanism in underlying neurophysiology and the alteration in the behavioral outcomes.

Changes in resting‐state functional brain connectivity associated with head impacts over one men’s semi‐professional soccer season

“…Resting‐state fMRI studies conducted in American high school football players over one or two football seasons, whether they sustained concussions, showed significant changes in fMRI, including a prolonged alteration in DMN, suggesting possible accrued RHSI‐related damage (Abbas et al., 2015; Breedlove et al., 2012). Only one fMRI study was conducted in female high school soccer players: significant pre‐ to postseason changes in fMRI brain activation were demonstrated when performing a working memory task (Yuan et al., 2018). No studies have assessed the relationship between soccer‐related RHSI exposure in trained male players and their brain function at rest.…”

The effects of internal jugular vein compression for modulating and preserving white matter following a season of American tackle football: A prospective longitudinal evaluation of differential head impact exposure

“…The degree of venous dilation is purported to be less than a human's natural physiologic response to a Valsalva maneuver, sneeze, or cough (Myer, Yuan, Barber Foss, Thomas, et al., 2016). Previous prospective longitudinal clinical trials have not reported any harm or injury related to collar wearing (Bonnette et al., 2018; Dudley et al, 2020; Myer et al, 2018; Myer, Yuan, Barber Foss, Smith, et al., 2016; Myer, Yuan, Barber Foss, Thomas, et al., 2016; Yuan, Barber Foss, et al., 2018; Yuan, Dudley, et al., 2018; Yuan et al., 2017), nor were any reported in the present study.…”

“…Although still an indirect measure of histopathology, DTI is capable of quantifying the characteristics of diffusion and anisotropic properties of water molecules within cerebral white matter microstructure (American College of Radiology, 2019; Soares, Marques, Alves, & Sousa, 2013). The technique has been used extensively to characterize white matter alterations in response to neurologic insult resulting from head trauma (Aoki, Inokuchi, Gunshin, Yahagi, & Suwa, 2012; Bahrami et al., 2016; Bazarian, Zhu, Blyth, Borrino, & Zhong, 2012; Bazarian et al., 2014; Chamard & Lichtenstein, 2018; Chun et al., 2015; Davenport et al., 2014; Eierud et al., 2014; Gajawelli et al., 2013; Inglese et al., 2005; Kuzminski et al., 2018; Marchi et al., 2013; Mayinger et al., 2018; McAllister et al., 2014; Merchant‐Borna et al., 2016; Mustafi et al., 2018; Myer et al, 2018; Myer, Yuan, Barber Foss, Smith, et al., 2016; Myer, Yuan, Barber Foss, Thomas, et al., 2016; Newcombe et al., 2007; Slobounov et al., 2017; Sollmann et al., 2018; Urban et al., 2013; Wallace, Mathias, & Ward, 2018; Yuan, Barber Foss, et al., 2018; Yuan, Dudley, et al., 2018). With respect to American football, a recent systematic review of prospective studies revealed that longitudinal changes in DTI metrics—specifically fractional anisotropy (FA) and mean/axial/radial diffusivity (MD, AD, RD)—were associated with high‐school athletes' cumulative exposure (quantity and magnitude) to head impacts experienced throughout their competitive season (Schneider et al., 2019).…”

“…Animal research has demonstrated that internal jugular vein compression (JVC) can increase cerebral vascular blood volume and thus minimize the effects of head impacts on brain injury (Mannix et al., 2020; Smith et al., 2011; Turner et al., 2012). In humans, JVC—using a neck “collar” that applies mild bilateral pressure to the internal jugular vein—is similarly theorized to increase cerebral venous engorgement, mitigate brain slosh, and has been successfully used in a series of preliminary longitudinal human clinical trials (Bonnette et al., 2018; Myer et al, 2018; Myer, Yuan, Barber Foss, Smith, et al., 2016; Myer, Yuan, Barber Foss, Thomas, et al., 2016; Yuan, Barber Foss, et al., 2018; Yuan, Dudley, et al., 2018; Yuan et al., 2017). Previous studies of the JVC neck collar have used tract‐based spatial statistics (TBSS; Smith et al., 2006) to quantify alterations in DTI‐derived diffusion and anisotropic properties of white matter, and found athletes who wore the collar during competitive play showed significantly fewer pre‐ to postseason changes compared to non‐collar wearing athletes despite comparable levels of head impact exposure (Myer et al, 2018; Myer, Yuan, Barber Foss, Smith, et al., 2016; Myer, Yuan, Barber Foss, Thomas, et al., 2016; Yuan, Barber Foss, et al., 2018).…”

“…The research studies supporting prospective, in vivo longitudinal JVC, however, were preliminary (single teams and small sample sizes), only controlled for total accumulated head impact exposure (i.e., cumulative frequency of head impacts for any magnitude >20 g) between collar‐wearing and non‐collar wearing groups, or did not use head impact data in the primary DTI analyses (Myer et al, 2018; Myer, Yuan, Barber Foss, Smith, et al., 2016; Myer, Yuan, Barber Foss, Thomas, et al., 2016; Yuan, Barber Foss, et al., 2018; Yuan, Dudley, et al., 2018). Specifically, prior JVC neck collar studies were not designed to systematically deconstruct whether the observed findings were consistent for athletes exposed to greater (or fewer) sub‐concussive head impacts, nor whether the actual magnitude of impacts uniquely contributed to findings.…”