Mild Traumatic Brain Injury: An Overview

CHAPTER 1

JAMES B. HOELZLE

KATHRYN A. RITCHIE

OVERVIEW

Although historically considered a common and relatively benign injury, mild traumatic brain injury (mTBI), or concussion,¹ has recently received extensive media attention. Once described by the Centers for Disease Control and Prevention (National Center for Injury Prevention and Control, 2003) as a “silent epidemic,” mTBI is now regularly discussed across disciplines and demographics. News stories routinely describe empirical research and atypical case studies suggesting there are possible short- and long-term risks associated with youth participation in contact sports. A great deal of attention has also been directed toward the Department of Veterans Affairs, focusing on how care is provided to service men and women who have sustained traumatic brain injuries while deployed overseas. Interestingly, committed fans of the National Football League are even drawn to controversies surrounding concussions, and some have a sophisticated understanding of medical protocols that are in place to protect players and determine when it is safe to return to play. It is clear that there is nothing “mild” about mTBI and our interest in it.

Although the literature suggests that a great majority of individuals recover from mTBI over the course of weeks to several months (e.g., Carroll et al., 2004), many clinicians recognize that recovery processes vary significantly from patient to patient, and a meaningful percentage of individuals who seek medical care in the postacute phase of recovery attribute a wide range of difficulties to mTBI. The body of literature describing risk factors, associated symptoms, and outcome from mTBI is quickly growing and sometimes appears to be contradictory. The present chapter is structured to provide sufficient background information to recognize some unique challenges associated with diagnosis and treatment of mTBI. A brief historical overview provides background and in part explains why well-respected and knowledgeable researchers and clinicians have reached different conclusions regarding the significance and outcomes associated with mTBI. The neurobiological mechanisms underlying mTBI, risk factors associated with extended recovery, and debates regarding recovery course and long-term cumulative impact of mTBI will also be discussed. Collectively, this information should help clinicians identify issues that might confound diagnosis and recovery from mTBI. Additionally, this information may be useful to share with patients when formulating treatment plans and discussing prognosis.

HISTORY

Although the term “concussion” has come to define the transient sequelae of symptoms associated with mTBI, particularly in the sports literature, it has been used colloquially for centuries, and its meaning has evolved over time. As early as 900 CE, the Latin term commotio cerebri was used in medical literature to convey a disruption in brain function without lesions or fracture (McCrory & Berkovic, 2001). In the generations that followed, the term “concussion,” likely derived from the Latin concutere, or “to shake,” was used to refer to an acute set of symptoms caused by “shaking” of the brain (McCrory & Berkovic, 2001).

Throughout the 20th century, the dominant perspective in the medical literature was that in most cases concussions were harmless and did not bear any long-standing effects on behavior (Bigler, 2008). In fact, any persisting symptoms associated with concussion were considered psychological relics of involvement in an accident or litigation, termed “accident neurosis” (Miller, 1961). The focus of concussion research in the 21st century, and perhaps the most elusive aspect of concussion research, has been to determine whether concussion results in transient functional disturbance with no enduring damage or whether there is lasting pathological damage via axonal shearing (McCrory & Berkovic, 2001). More recent research has also aimed to identify a minimum necessary biomedical threshold of impact to produce mTBI and evaluate potential long-term implications associated with the cumulative effects of multiple concussions.

A significant number of challenges are associated with studying mTBI. For one, there have been only a few controlled, prospective studies of the acute injury characteristics of mTBI (McCrea, 2008). Those that do exist often have small sample sizes, or low generalizability for various reasons. For example, studies that include individuals involved in accidental falls or motor vehicle accidents (MVAs), in the absence of eyewitnesses, may inaccurately report event parameters or acute injury characteristics (e.g., loss of consciousness; posttraumatic amnesia) that help quantify injury severity. Additionally, symptom reporting may be influenced by secondary gain issues and ongoing litigation. The significance of this issue cannot be understated. For example, after controlling for injury severity and premorbid factors, individuals involved in litigation report more significant symptoms, social dysfunction, and poorer outcome relative to those who are not pursuing compensation (see, for example, Feinstein, Ouchterlony, Somerville, & Jardine, 2001; Paniak et al., 2002).

A positive development in understanding mTBI and the natural course of recovery was the recognition that observing athletic participation is in many ways an ideal and rigorous natural laboratory. It is well documented that a significant number of athletes will sustain a concussion while participating in their respective sports. Postinjury neurocognitive performance relative to preseason baseline performances allow one to fully appreciate and quantify neurocognitive issues associated with mTBI. Additionally, injuries occur in individuals who are most likely young and healthy, and motivated to recover quickly. In other words, many of the confounding factors that are associated with MVAs (e.g., litigation) and unreported falls (e.g., no collateral information defining injury parameters) are not present in athletes who sustain concussion (McCrea, 2008).

For decades, research has been conducted to quantify the effects of sports-related concussion. Belanger and Vanderploeg (2005) conducted a meta-analysis of this literature and reported that it is common to observe decreased neurocognitive functioning in athletes during the first 24 hours postinjury. Encouragingly, full neuropsychological recovery is typically observed within 7 to 10 days in athletes. Although beyond the scope of the current work, collectively, this study, those contributing to it, and many others have made it possible to develop evidence-based guidelines for injury diagnosis, evaluation, and return-to-play decisions (e.g., Echemendia, Giza, & Kutcher, 2015; McCrea, Broshek, & Barth, 2015). Nevertheless, despite these positive developments, some researchers have questioned whether information obtained during sports concussion research can be generalized to nonathletes. For example, some have correctly pointed out that athletes likely have a variety of protective factors, which may include both physiological (i.e., better developed neck musculature) and psychological attributes (i.e., motivation to return to play, symptom underreporting), that increase the likelihood of rapid and positive recovery (Rabinowitz, Li, & Levin, 2014).

PATHOPHYSIOLOGY

Numerous attempts have been made to identify the minimum threshold of force (g-force) necessary for mTBI. Innovative technology has been developed to record linear head acceleration at impact and makes clear that a positive relationship exists between magnitude of impact and the probability of mTBI. Although it has been proposed that a range of 80 to 100 g is a minimal biomedical threshold sufficient to cause mTBI (McCrea, 2008), Zhang, Yang, and King (2004) established that there is a 25% chance of mTBI with 66 g, 50% chance with 82 g, and 80% chance with 106 g. Additionally, it is recognized that the addition of rotational forces greatly increases the odds of mTBI (Ommaya & Gennarelli, 1974).

Despite a seemingly plausible threshold of mechanical force for injury, there is not clear evidence that affect magnitude (linear or rotational acceleration), or affect location, is meaningfully related to acute clinical outcome (Guskiewicz et al., 2007). Once an injury threshold is exceeded, a neurometabolic cascade of complex physiological events may adversely affect cerebral functioning for days to weeks by affecting intracellular and extracellular concentrations of potassium, sodium, calcium, and magnesium ions (Giza & Hovda, 2004). A complex chain of ionic, metabolic, and physiological events is thought to render neurons dysfunctional as opposed to destroyed (McCrea, 2008).

There is a strong desire to pursue “objective” hallmark neurophysiological sequelae of mTBI using traditional and novel neuroimaging methods. Although this has proven to be somewhat challenging, attempts to do so have resulted in a better understanding of the relationship between injury severity and outcome. It is important to recognize that although CT scans are commonly obtained in emergency departments (EDs) to rule out hemorrhagic lesions or structural injury, the method has poor sensitivity to detect abnormalities typically associated with mTBI. Advanced MRI and DTI approaches appear to be more effective in detecting neuropathology associated with mTBI, including miniscule hemorrhages and diffuse axonal injury (e.g., Belanger, Vanderploeg, Curtiss, & Warden, 2007; Chastain et al., 2009). fMRI research also provides evidence that structures mediating working memory are affected by mTBI (e.g., McAllister, Flashman, McDonald, & Saykin, 2006). In terms of patient outcome, there is an important distinction between normal and abnormal imaging. The latter results in a classification of “complicated mTBI” and increases the risk for delayed or incomplete recovery (e.g., Iverson, Brooks, Collins, & Lovell, 2006).

ETIOLOGY

A major challenge in studying mTBI is the heterogeneous nature of injuries sustained (Cassidy et al., 2004). As the majority of mTBIs are associated with various types of accidents, many factors can complicate recovery, including other orthopedic and neurological injuries, involvement in litigation, and premorbid psychiatric factors. These issues are typically less relevant in the context of sports-related concussion (SRC). As such, the scientific literature typically distinguishes mTBIs into sport and nonsport etiologies, but the degree to which the etiologies are interrelated is uncertain (Rabinowitz et al., 2014).

Traumatic brain injury (TBI) is most frequently attributed to blunt-force trauma or closed-head injury. Blunt-force trauma occurs when the head hits a fixed object or when a moving object strikes the head. Blunt-force trauma occurs most commonly because of MVAs, accidental falls, assaults, sports injury, or other accidents (Roberts & Roberts, 2011). In most instances of blunt-force trauma, the force of the impact is transferred from the skull to the brain, without breaking the skull, though an impact can still be considered a closed-head injury if the skull is fractured and the meningeal covering of the brain is not punctured (Lezak, Howieson, Bigler, & Tranel, 2012). Throughout the life span, most TBIs are due to accidental falls (35.2%). According to the CDC, the second most common etiology is due to MVAs (16.5%), followed by being hit by or against an object (16.5%), and assaults (10%) (Faul, Xu, Wald, & Coronado, 2010).

Military combat also presents a common etiology for mTBI. Although blunt-force trauma has long been understood as a source of combat-related mTBI, in light of Operation Iraqi Freedom (OIF) and Operation Enduring Freedom (OEF), recent research attention has focused on the symptom sequelae associated with blast-related mTBI. As OIF and OEF have presented new warfare tactics, including exposure to improvised explosive devices (IEDs), an understanding of blast-related TBI is somewhat less developed relative to other areas of TBI research. Noteworthily, there is some neuroimaging evidence that suggests the neuropathology of blast-related TBI may differ from that of blunt-force trauma (Warden et al., 2009).

SRC also constitutes a sizable proportion of all mTBIs reported annually. In American collegiate athletes, 6.2% of all sports injuries were mTBIs (Covassin, Swanik, & Sachs, 2003). Team contact sports such as hockey and football may have the highest rates of SRC per year, though there is great in-sport variability in the estimated incidence of concussion in individual sports (Schulz et al., 2004).

EPIDEMIOLOGY

TBI is one of the most common health conditions in the United States, with prevalence estimates between 1.4 and 3 million cases per year (Summers, Ivins, & Schwab, 2009). It is estimated that mTBIs make up 70% to 90% of all TBI cases reported to EDs annually (Cassidy et al., 2004). Because of its high prevalence rate and associated societal cost, TBI is a very significant public health concern.

Because of the unique factors associated with mTBI, it is somewhat challenging to determine epidemiological rates and risk factors associated with the condition. A systematic review of incidence and risk factors associated with mTBI reveals great heterogeneity among published mTBI studies based on inclusion criteria and the manner in which mTBI is operationalized (Cassidy et al., 2004). Because there is not a universally agreed-upon definition of mTBI (described in greater detail in the following sections), it is difficult to estimate true incidence and prevalence rates, especially in less severe cases of mTBI. Another factor complicating accurate epidemiological rates is the fact that mTBI is severely underreported (McCrea, 2008). Most incidence rate studies rely only on ED reports, but one study has estimated that approximately 25% of the population did not seek medical attention after sustaining mTBI (Sosin, Sniezek, & Thurman, 1996). Although review of the literature suggests incidence rates of 100 to 300/100,000 adults, studies that included self-reported mTBI observed incidence rates as high as 600/100,000 (Cassidy et al., 2004). It will be interesting to see whether these incidence rates increase in the future with greater societal awareness of mTBI.

Though it has been difficult to determine distinct risk factors across the heterogeneous literature, some crude epidemiological trends have emerged. For instance, male patients account for approximately two-thirds (59%) of all reported cases (American Psychiatric Association [APA], 2013; Summers et al., 2009). Additionally, mTBIs exhibit a unique, bimodal age distribution, occurring most frequently in late childhood and adolescence, and then again in later adulthood (APA, 2013; McCrea, 2008) (see Chapters 13 and 14). This pattern indicates that mTBI affects people across the life span and that there are many developmental considerations to take into account when assessing for and treating concussions. Finally, a higher incidence of mTBI is reported by minorities; however, it has been difficult to distinguish whether these observed differences can be attributed to race or other risk factors for mTBI, such as socioeconomic status (McCrea, 2008).

As previously noted, another common cause of mTBI is SRC. The Centers for Disease Control and Prevention reported an annual incidence of approximately 300,000 SRCs, though this number is likely a conservative estimate because as many as half of all SRCs remain unreported (McCrea, Hammeke, Olsen, Leo, & Guskiewicz, 2004). Cumulatively, SRC is responsible for about 20% of all reported TBIs annually (Bailey, McCrea, & Barth, 2013). It is certainly plausible that this number will increase in the future as athletes, coaches, parents, and athletic trainers become more aware of symptoms associated with concussion. The incidence of mTBI is also high within the military population as it is the most common injury associated with recent military involvement (Hoffer, Donaldson, Gottshall, Balaban, & Balough, 2009). In fact, between 2000 and 2012, more than 244,000 military personnel were diagnosed with TBI, and 80% of the injuries were considered mild in nature (Defense and Veterans Brain Injury Center, 2012).

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