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Sport-related Concussion Clinical Profiles

Clinical Characteristics, Targeted Treatments, and Preliminary Evidence

Kontos, Anthony P., PhD1,2; Sufrinko, Alicia, PhD1,2; Sandel, Natalie, PsyD2; Emami, Kouros, PsyD2; Collins, Michael W., PhD1,2

Current Sports Medicine Reports: March 2019 - Volume 18 - Issue 3 - p 82–92
doi: 10.1249/JSR.0000000000000573
Chest and Abdominal Conditions/Special Communication
Free

Sport-related concussion (SRC) is a heterogeneous injury that involves varied symptoms and impairment that presents a significant clinical challenge to sports medicine professionals. In response to this challenge, clinical researchers have proposed clinical profiles or subtype models for assessing and treating athletes with SRC. One such model emphasizes five concussion clinical profiles including cognitive/fatigue, vestibular, ocular, migraine, and anxiety/mood. Sleep is a common modifier that co-occurs across these clinical profiles. A combination of medical history, risk factors, injury information, clinical characteristics, and assessment outcomes can inform each clinical profile. Preliminary data involving 236 patients from a concussion specialty clinic indicate that the migraine (26%) and anxiety/mood (24%) profiles are the most common, with vestibular and ocular profiles combined representing more than one third (35%) of clinical profiles. Findings also support several relationships among different clinical profiles including vestibular and migraine, suggesting that many athletes present with multiple clinical profiles. Targeted, active treatments for each profile are discussed.

1Department of Orthopaedic Surgery, University of Pittsburgh, Pittsburgh, PA; and

2UPMC Sports Medicine Concussion Program, Pittsburgh, PA

Address for correspondence: Anthony Kontos, PhD, UPMC Rooney Sports Complex, 3200 South Water St., Pittsburgh, PA 15203; E-mail: akontos@pitt.edu.

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Introduction

Sport-related concussion (SRC) is a major health concern affecting millions of athletes each year in the United States alone, including up to 1.9 million children and adolescents (1). SRC involves a variety of symptoms (e.g., somatic, cognitive, sleep, affective) and functional impairments (e.g., balance, cognitive, gait, ocular, vestibular) (2). Consequently, SRC does not present clinically in a consistent manner, resulting in a heterogeneous injury that poses a unique challenge to sports medicine professionals. Therefore, an approach to management, such as prescribed rest, will not be effective for all athletes with SRC and may actually harm some athletes (3). In fact, there is a shift in the approach to evaluating and treating SRC that emphasizes active and targeted treatment based on specific symptoms and impairment (4). Recent research suggests that sports medicine professionals applying an SRC treatment strategy—even prescribed rest—must consider the characteristics of the injury and athlete alike (5,6).

To address the heterogeneity of this injury and improve clinical care, researchers have proposed clinical profile-based approaches to conceptualize SRC (7–9). These approaches are designed to inform both assessment and more targeted and effective therapies for athletes with SRC. Although these approaches were originally developed in concussion specialty clinics, they can be applied to inform better assessment and care in a variety of environments, including primary care, pediatric, and emergency medicine. The purpose of this article is to describe and update the evolving clinical profile-based conceptual model for concussion from Kontos and Collins (9) and Collins and colleagues (7). In addition, this article will examine preliminary evidence for the prevalence of each clinical profile, association among different profiles, and clinical characteristics of athletes with each profile.

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Concussion Clinical Profiles

In 2014, Collins and colleagues (7) proposed a clinical model that conceptualized concussion from a heterogeneous perspective. This model, which is described in detail by Kontos and Collins (9), includes six different clinical trajectories or profiles: 1) cognitive/fatigue, 2) vestibular, 3) ocular, 4) posttraumatic migraine, 5) anxiety/mood, and 6) cervical. Since the introduction of this model, cervical— which is not cerebral concussion per se—has transitioned to represent a modifier along with sleep. As such, while it is important to assess cervical function and symptoms when evaluating and treating athletes following concussion, only a brief note about this clinical profile/emerging modifiers is provided in the current article. We will focus in more depth on the five cerebral concussion clinical profiles and sleep-related problems that might accompany a concussion. However, before diving into the profiles themselves, it is important to provide some context for the way in which the clinical profiles are applied.

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Determining Clinical Profiles: Prioritization, Overlap, and Risk Factors

There are several challenges to determining an athlete’s clinical profile following concussion. In some instances, athletes may present with a single, clearly defined clinical profile in the absence of other profiles. However, athletes typically present with more than one clinical profile (7). Therefore, sports medicine professionals must first prioritize each identified concussion clinical profile described in the following sections as primary, secondary, or tertiary. This prioritization of concussion clinical profiles should be informed by a comprehensive assessment of symptoms and impairment that includes multiple domains, such as affective, balance, cognitive, ocular, and vestibular. Such an assessment should incorporate medical history, including risk factors and injury information, clinical examination and interview, symptom reports, and testing and screening for impairment (e.g., balance, cognitive).

The clinical challenge of prioritizing concussion profiles is complicated further by the fact that profiles may overlap and share some clinical characteristics. For example, dizziness could occur in athletes with both migraine and vestibular clinical profiles, and both ocular and cognitive/fatigue profiles may involve attentional and visual processing difficulties (7). Another challenge facing sport medicine professionals is obtaining a detailed medical history and injury information to determine the influence and interplay among potential primary (i.e., preinjury) and secondary (i.e., postinjury) risk factors for each clinical profile. For instance, an athlete with a family history of migraine may be more likely to have a postinjury migraine clinical profile than an athlete without a history of migraine, per recent findings (6). Sufrinko and colleagues (6) highlighted the need to identify not only personal but also familial history of risk factors, such as migraine. Finally, a thorough history of relevant risk factors also should include information about subclinical, that is, below the threshold of formal medical diagnosis-symptoms (e.g., headache, depression, anxiety). These subclinical symptoms are particularly relevant when evaluating younger athletes who may not yet be diagnosed or lack insight into the relevance of their symptoms.

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Overview of Clinical Profiles

An overview of the clinical profiles, including common symptoms, clinical examination/evaluation findings, risk factors, and targeted treatment strategies is provided in Table 1. More nuanced descriptions of each clinical profile and the sleep modifier are provided in the following sections.

Table 1

Table 1

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Cognitive/fatigue

The cognitive/fatigue profile is characterized by predominant complaints of difficulty with cognitive or thinking skills and pronounced fatigue when engaged in mental activities. Symptoms associated with this profile include trouble concentrating, memory problems, feeling mentally slow or foggy, fatigue, and low levels of energy. It is well established that many athletes experience transient cognitive decline after sustaining an SRC (10–13). Some athletes may recognize cognitive problems, while others may not notice overt changes in mental capacity, but exhibit deficits in attention and memory processes when evaluated on objective neurocognitive testing (14–16). In addition to cognitive difficulties, these athletes also may endorse a nonspecific headache, fatigue toward the end of the day, and a disruption of their sleep schedule (5). Associated functional impairments include difficulty upholding academic and/or occupational responsibilities due to decreases in cognitive efficiency and inability to sustain productivity in these environments (17,18).

To determine if an athlete is exhibiting the cognitive/fatigue profile, a thorough assessment of symptoms and cognitive functioning is warranted. The clinical interview should be targeted at evaluating academic and occupational performance while symptom inventories can evaluate the presence and severity of perceived cognitive complaints. Subjective symptom reports should always be compared with objective neurocognitive testing of multiple cognitive domains, including memory, attention, executive functioning, and processing speed (17,19). Risk factors for the development of this clinical profile after SRC are largely unknown, but may include continuing to play following a concussion as well as continuing daily activities despite symptom provocation. Also, athletes with neurodevelopmental conditions may be more predisposed to deficits in cognition after head injury consistent with literature on the concept of cognitive reserve (20). For instance, athletes with a history of an attention or a learning disorder demonstrated reduced cognitive performance relative to healthy controls on cognitive screening tools for concussion prior to injury (21,22), and therefore, may have less cognitive reserve or resiliency against cognitive impairment after SRC. Another potential risk factor for the development of the cognitive/fatigue profile after SRC includes poor-quality sleep prior to injury (23).

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Vestibular

The vestibular system is a complex sensory network that provides information to the brain about motion, equilibrium, and spatial orientation to maintain balance and interpret movement in the environment. Central vestibular pathways receive information from multiple sources including the peripheral vestibular organs, visual pathways and proprioception, and integrate this sensory information to direct motor output to maintain postural stability and vestibular-oculomotor reflexes (24). A disruption of vestibular function results in symptoms of motion sickness such as dizziness, lightheadedness, imbalance, nausea, and fogginess. Nearly half of athletes after SRC report balance problems or dizziness that are characteristic of the vestibular profile (25,26). Athletes with the vestibular clinical profile may be asymptomatic when at rest, but also may experience a provocation of symptoms when engaged in dynamic movement (e.g., sport participation), activities involving motion (e.g., car rides), and/or when in crowded environments. Some athletes may develop concomitant anxiety and feelings of detachment/dissociation along with vestibular dysfunction, because there are close relationships between the vestibular system and mood changes (27–29). The vestibular clinical profile is associated with a longer recovery time from SRC (30) and may require targeted vestibular therapies (31,32) for full symptom resolution.

Evaluation of the vestibular clinical profile requires a behavioral assessment of symptoms during the clinical interview and screening of vestibular-oculomotor function. Questions during the clinical interview should be targeted at determining the activities that provoke symptoms (e.g., “when you engage in dynamic (i.e., involving head movement) physical activity, do you notice an increase in symptoms?”) and those activities that are being avoided due to symptom provocation (e.g., athletes avoiding the school cafeteria due to feeling overwhelmed in a busy environment). Athletes’ report of symptoms should be verified with comprehensive vestibular-oculomotor screening. Screening tools designed for evaluating vestibular dysfunction after SRC include assessments of smooth pursuits, saccades, vestibular-ocular reflexes, and visual motion sensitivity (33,34). Balance testing also is recommended in the acute phase of injury to evaluate vestibular integrity, but may not be sensitive to SRC beyond 3 d postinjury (35,36). Recent research indicates that a potential risk factor for the development of this clinical profile after SRC is a preinjury history of high susceptibility toward motion sickness (37).

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Ocular

The ocular profile is characterized by posttraumatic vision impairment and related symptoms. Athletes with SRC can experience oculomotor dysfunction, such as deficits in convergence and accommodative functions that facilitate maintenance of near vision (38–41). Symptoms indicative of the ocular profile include complaints of blurred or double vision, trouble focusing, frontal headache or pressure, and fatigue with visual activities, such as reading or computer work. Academic and occupational functioning may be affected when there is an oculomotor deficit given the demand on vision in these environments (42).

Assessment of the ocular profile following SRC requires screening of oculomotor functions, including smooth pursuits, saccades, near point of convergence, and accommodation (33,43). Athletes diagnosed with a vision disorder after SRC are at risk of prolonged recovery time (44). In addition to directly evaluating oculomotor function, other assessment tools within a multimodal evaluation may provide supporting evidence for an ocular deficit. For instance, athletes with a convergence insufficiency (CI) exhibit a lowered performance on computerized neurocognitive testing (40,41) and report higher symptoms on questionnaires of visual function (40). There are no known risk factors associated with the ocular profile, but it is speculated that a preinjury history of an oculomotor abnormality (e.g., strabismus) may render athletes more susceptible to exhibit the ocular profile after SRC (7).

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Migraine

A posttraumatic migraine is defined as a moderate-to-severe, pulsating headache after head trauma that is accompanied by symptoms of nausea and/or photosensitivity and phonosensitivity (45). The most commonly reported symptom after SRC is headache, and most athletes will endorse symptoms consistent with migraine in the first week of the injury (25). However, athletes exhibiting the migraine profile may experience a persistent, intermittent headache beyond this timeframe (46,47). Other potential symptoms associated with this profile include sleep dysregulation (48) and anxiety/mood disturbance (49). Athletes may report a worsening of headache when under stress or when engaged in physical activity (45). There is an increased risk of prolonged recovery time from SRC when athletes experience migraine symptoms, and these athletes may have difficulty tolerating functional activities (46,47).

To determine the presence of this clinical profile, a thorough evaluation of headache characteristics should be conducted as part of the clinical interview. The features of the headache and associated symptoms provide valuable information regarding the nature and classification of the headache. Information on the following headache characteristics can help to determine if an athlete meets the classification for migraine clinical profile: severity, frequency, onset, triggers, location, duration, quality/sensation (e.g., pulsating, throbbing, sharp pain), accompanying symptoms (e.g., nausea), and presence/absence of an aura. Athletes exhibiting the migraine profile also demonstrate decline across memory and speed composites of neurocognitive testing (46). A personal or family history of migraine may predispose athletes to demonstrate this clinical profile (50) after SRC.

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Anxiety/mood

The anxiety/mood clinical profile is associated with emotional and behavioral changes after injury. Indicators of the presence of this profile include reports of depression, anxiety, feeling more emotional, moodiness, or irritability. Some athletes may not overtly describe emotional changes, but may exhibit behavioral manifestations that are characteristic of an underlying psychological disturbance (e.g., avoidant coping, ruminative thinking, hypervigilance) (51,52). Other associated features of the anxiety/mood clinical profile may include sleep dysregulation, exaggerated or inconsistent somatic symptoms, and physiological alterations of the autonomic nervous system (8,53).

Evaluation of this clinical profile requires a sophisticated understanding of the typical signs and symptoms of SRC, as well as an appreciation for both the physiological and psychological aspects of the injury. Through a clinical interview and symptom questionnaires of emotional functioning, the level and nature of emotional distress can be evaluated after the injury. However, it also is important to consider the role that mental health may be playing in presentation of physical symptoms; this is not always a straightforward task as athletes may not recognize how psychological processes may influence perception and reporting of somatic symptoms and/or do not want to accept a psychological explanation for physical symptoms. Indicators of an underlying emotional disturbance include inconsistent symptom reporting, discrepancies in subjective complaints and performance on objective neurocognitive testing, and a worsening of symptoms over time (54–56). The presence of a preinjury history of mental health disorder is one of the strongest predictors of a prolonged recovery from SRC (57–59), and a risk factor for the development of the anxiety/mood clinical profile after injury (60–62).

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Brief Note About Cervical as a Modifier of SRC

SRC may involve cervicogenic injury due to the neck’s role in stabilizing the head. Although this clinical profile has evolved into a modifier in the current model, it is important to always evaluate the neck following any SRC. Such an evaluation should be performed by a physician or physical therapist with expertise in cervical assessment. Cervical symptoms may include neck pain or stiffness, limited range of motion or strength in the neck, headache (often originating toward the back of the head), and numbness or tingling. Sleep also may be disrupted as a result of cervical pain and discomfort, leading to impaired recovery. If a cervical modifier is confirmed, appropriate referrals to a physical medicine and rehabilitation physician and physical therapist who specializes in cervical rehabilitation should be initiated.

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Sleep as a Modifier of SRC

Sleep problems are one of the most common complaints following SRC, affecting 30% to 70% of patients (63,64), and may be predictive of prolonged recovery following SRC (65). Few studies to date have examined sleep in the acute stage of SRC recovery, and most have focused on nonsport injuries. Physical (e.g., fatigue, headache), cognitive (e.g., problems concentrating, poor academic performance), and emotional symptoms (e.g., irritability, anxiety) of inadequate sleep in healthy athletes (66,67) may mimic concussion sequelae, thereby complicating determination of symptom-free status postinjury. As such, it is important to consider the etiology, prevalence, and characteristics of sleep problems following SRC and how sleep issues may impact athletes’ concussion clinical profiles.

Sleep complaints following SRC have a complex etiology and poorly understood pathophysiology. It has been posited that the diffuse axonal injury that results from concussion preferentially affects midline structures that directly affect sleep-wake mechanisms, including the deep gray matter, dorsolateral pons, and midbrain (67). Reduced activation of the prefrontal cortex has been implicated in sleep deprivation (68), as well as following SRC (69), suggesting a potential mechanism for sleep-related symptoms (23). Further, the neurometabolic cascade may affect the release of neurotransmitters, such as melatonin, that are involved in the regulation of sleep-wake circuits (67). Interestingly, studies to date have failed to find “objective” evidence of sleep disruption to support subjective sleep complaints following SRC. In a study examining overnight polysomnography of athletes who sustained a concussion in the past year compared with controls, no differences in objective sleep characteristics were observed despite the SRC group reporting reduced sleep quality (70). In a recent study examining sleep parameters with actigraphy throughout the first few weeks following SRC, athletes decreased the amount of time spent in bed throughout recovery, but sleep duration did not change (71). Both of these studies were limited by small sample sizes, but nonetheless underscore the subjective nature of concussion symptoms.

Following a concussion, patients often report sleep onset and maintenance problems, as well as hypersomnia and excessive daytime sleepiness (70). Sleep difficulties also can change throughout the course of recovery, supporting the notion that sleep problems have a multifactorial etiology. In the acute stage of injury the underlying pathophysiology may be a root cause for sleep problems, although an adjustment response, such as not sleeping due to worry about missing an upcoming game, also is a plausible contributing factor influencing sleep difficulties (72). Although many athletes with SRC report difficulty sleeping, some athletes, especially adolescents, may engage in modifiable behaviors (e.g., socializing, late night electronics use, completing homework late at night) that could directly affect sleep. Changes in normal sleep patterns associated with prescribed rest also can disrupt the sleep-wake schedule and result in an iatrogenic problem (73). Further, preinjury vulnerability to sleep problems may differ across athletes. In fact, preinjury sleep difficulties on baseline assessment were shown to be associated with worse sleep problems, larger magnitude of cognitive impairment and overall higher symptom scores in the first few weeks following SRC (23).

Sleep problems following SRC are unique in that they represent both a natural consequence of injury and a modifiable behavior affecting recovery. Sleep factors can directly influence the manifestation of clinical profiles following SRC. The influence of sleep on the mood/anxiety profile is perhaps the most intuitive, and the bidirectional relationship between psychopathology and sleep is extensively documented among individuals without history of SRC (74). Several studies acknowledge that sleep problems and emotional symptoms often co-occur following SRC (7,75,76). For example, researchers have reported that patients with sleep onset insomnia following concussion also have higher anxiety scores, and patients with sleep maintenance insomnia have higher depression scores (77). Similarly, there is reciprocal relationship between migraine and sleep (78), as migraine symptoms are known to trigger sleep problems. In a recent study, researchers reported that sleep disturbances were correlated with greater report of migraine symptoms during the acute and prolonged phase of recovery (79). Both preinjury (23) and postinjury sleep problems (79) are associated with cognitive complaints and cognitive impairment following SRC, suggesting that inadequate sleep may play a role in the manifestation of cognitive/fatigue clinical profiles. Researchers using animal models have reported that the vestibular system is involved in regulation of circadian rhythms via the visual and somatosensory systems (80). Findings from a recent study indicated that nonconcussed individuals with vestibular complaints (i.e., vertigo) were more likely to report abnormally short or long sleep duration compared with individuals without vertigo (81). Given this finding, it is feasible that athletes with primary vestibular clinical profiles following SRC may be at risk for sleep problems postinjury. Finally, researchers have suggested that sleep deprivation in healthy adults can induce ocular dysfunction, including impaired pursuit and saccadic tasks (82,83). As such, ocular dysfunction may be exacerbated in SRC patients with inadequate sleep.

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Preliminary Data for Clinical Profiles

The clinical profiles model described previously has yet to be examined empirically. Therefore, we recently conducted a preliminary investigation of the clinical profiles model in our concussion specialty clinic to: 1) determine the frequency of each primary clinical profile and 2) examine the association among different profiles. An overview and the key findings from these preliminary data are provided in the sections that follow.

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Study overview

The study was a retrospective, blind review of patient clinical charts from two concussion specialty clinic sites in the mid-Atlantic region of the United States. Blind reviews were conducted by six clinicians comprised of three neuropsychologists and three physical therapists. For each patient, clinicians determined the primary and secondary clinical profiles based on relevant medical history, injury information, clinical interview/examination notes, reported symptoms, and cognitive and vestibular/ocular test results. Inclusion criteria for participants included: first clinic visit; a diagnosed concussion with a clear mechanism of injury, current symptoms, and/or impairment; 11–40 years in age; complete clinical chart data for clinical examination/interview notes, symptoms, and neurocognitive and vestibular/ocular test results. Patients were excluded if they met any one or more of the following criteria: history of moderate-severe traumatic brain injury, epilepsy, seizure disorder, stroke, major psychiatric disorder; no clear mechanism of injury; >90 d from injury; and non-English speaking. A total of 236 (69.4%) of 340 patient charts met study criteria and were included in the analysis. Participants included 139 (58.9%) females and average age was 19.11 years (SD = 7.1 years). The average time since injury for participant was 15.3 d (SD = 16.1 d). A total of 33.1% (n = 78) of participants were 7 d, 44.5% (n = 105), 8 to 21 d, and 22.5% (n = 53), 22 to 90 d postinjury.

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Frequency of clinical profiles

A summary of the frequency of primary profiles is provided in Figure. As is evident from Figure, the most common single primary profile was migraine, representing slightly more than one quarter of participants. The anxiety/mood profile was the second most common with just under one quarter of participants. Cognitive/fatigue was the least common primary profile. Over one third of participants had either vestibular or ocular primary profiles. These findings highlight the importance of a comprehensive concussion assessment comprising multiple domains including symptoms, cognitive, vestibular, ocular, and affective. The findings also highlight the heterogeneous presentation of SRC, with strong distribution of patients across profiles. The 26% of patients with the migraine clinical profile, which has been associated with prolonged recovery (46), may represent the minority of patients who take longer than normal to recover from this injury. The fact that the vestibular and ocular clinical profiles combined represented 35% of concussions highlights the relevance of assessing these domains when evaluating athletes with SRC. Given that vestibular and ocular symptoms and impairment are amenable to targeted vestibular and vision therapies (84), more than one in three patients may benefit from such an active treatment approach following concussion. The large number of patients with anxiety/mood clinical profiles emphasizes the need for including mental health professionals as part of a multidisciplinary approach to care for athletes with SRC. Finally, the challenges associated with identifying clinical profiles following concussion are evident in that 4% of the patients did not have a clear primary clinical profile.

Figure 1

Figure 1

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Associations among different clinical profiles

Using the same database described above, we conducted a series of χ2 analyses with odds ratios (OR) to determine the association of each primary profile with each secondary profile compared with all other profiles. Significant results from these analyses are provided in Table 2. Significant associations were supported among all primary concussion clinical profiles and at least one secondary profile, with the exception of the cognitive/fatigue primary profile. Specifically, athletes whose primary clinical profile was ocular were more likely to have a secondary cognitive/fatigue profile. This is not surprising, as previous research has supported a relationship between CI and impaired computerized neurocognitive test scores (41).

Table 2

Table 2

The finding also suggests two secondary profiles are particularly common among those with primary vestibular dysfunction. A reciprocal association between the vestibular and migraine profiles had been previously reported in the SRC literature. Specifically, researchers reported that posttraumatic migraine was associated with higher symptom provocation on vestibular/oculomotor screening (6). There may be physiological underpinnings for a complex relationship between vestibular dysfunction and onset of migraine among concussion patients. Vestibular migraine, characterized by a combination of vertigo, dizziness, and balance disturbance with migraine, is poorly understood. There is research suggesting neuroanatomical connections between the vestibular system and nociceptive brainstem areas responsible for migraine, as well as hypotheses surrounding hyperexcitability of the vestibular system in migraine patients (85). The vestibular primary clinical profile also was associated with a secondary ocular clinical profile, suggesting that these two common profiles may co-occur in athletes. This is not surprising provided the shared neuronal networks among vestibulo-ocular and optokinetic reflexes (86). Further, symptoms in these profiles often overlap, posing challenges to treating clinicians. For example, dizziness can occur with reading in a concussed or healthy individual with only oculomotor dysfunction (87), and blurred vision is a common complaint with quick head movements due to vestibular dysfunction (88) in the absence of oculomotor findings.

The migraine secondary clinical profile was also associated with the primary anxiety/mood clinical profile. Although there are no known studies examining the relationship between migraine and mood within the SRC literature, there are several studies that indicate anxiety and migraine are common comorbidities (89), and stress is often a trigger for migraine (90,91). These preliminary findings provide some support for associations among primary and secondary clinical profiles following concussion. However, additional research to explore the relationships among the different clinical profiles and the underlying mechanisms for these relationships is warranted.

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Targeted and Active Treatment Approaches

Prescribed physical and cognitive rest has been the predominant recommendation to manage athletes following SRC (73). Given the pathophysiological and cerebrovascular changes that occur immediately following SRC (92), prescribed rest during this period is intuitive and also reduces the possibility of further insult to the already vulnerable brain. However, this approach to symptom management has fallen out of favor in lieu of a more active approach to symptom management in recent years. This shift has largely been in step with limited research supporting the effectiveness of the rest-based approach (93,94). In fact, prolonged rest can be detrimental and may lead to protracted recovery, especially in athletes who can become physically deconditioned following an extended period of rest. In addition, athletes may become socially isolated from their typical sport environment and experience other comorbid psychiatric issues including anxiety and depressed mood (3,95,96). Examples of these issues also have been identified with other medical conditions and animal models (97,98). In turn, arguments for more active treatments have garnered the attention of researchers and clinicians working with this patient population.

The most recent consensus statement by the Concussion in Sport Group still indicates that a brief period of prescribed cognitive and physical rest during the acute phase (i.e., 24–48 h), including increased sleep, is warranted following SRC (2). However, beyond this point, patients are being encouraged to gradually return to some degree of daily activity, which has been associated with improved outcomes (99). In 2016, another progressive statement was published that concluded “concussion is a treatable injury that should be approached in an active manner” (4) following a meeting among prominent experts in the field. Examples of active interventions include vestibular, vision, and exertion-based therapies, which have all shown promise in the literature (31,42,100,101). This level of specificity requires a multidisciplinary team that is adequately trained in the assessment of SRC and can make the proper recommendations.

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Behavioral management strategies

Beyond formal therapies, there are several basic behavioral recommendations that help with symptom management, but are still focused on recovery and rehabilitation. A regulated behavior plan that addresses positive lifestyle changes, including adequate diet/hydration, some degree of daily activity (i.e., noncontact physical activity), regulated sleep, and stress management (102), should be the cornerstone for an effective treatment plan for athletes following SRC. In a recent randomized controlled trial, researchers reported that adolescent patients who were provided with a clear and detailed behavioral management plan rather than being assigned to a strict rest treatment paradigm experienced fewer postconcussive symptoms (3). These same behavioral management strategies are applied and often recommended by health care practitioners managing nonconcussion-related headaches/migraines (103). Given that migraine is the most common clinical profile following concussion as reported earlier, it would seem imperative for clinicians managing this injury to educate their patients about the importance of adherence to these behavioral strategies. Further, increasing one’s daily activity can foster social interactions with peers and colleagues and in turn, reduce one’s likelihood to develop feelings of isolation and psychosocial stress.

Another functional rehabilitation strategy is an expose-recover model for symptom management following SRC. This approach is adopted from the well-established behavior theory of systematic desensitization (104) and may be applicable across all clinical profiles. Patients are encouraged to engage in (“expose”) activities, situations and environments (e.g., shopping malls, grocery stores, parties, etc.) that provoke or increase postconcussive symptoms for short durations with a subsequent period for recovery for symptoms to subside (56). It is hypothesized that with repeated exposures to provocative stimuli, symptoms will gradually lessen in severity and duration with eventual progression to extinction. Conversely, avoidance to these exposures may lead to symptom maintenance, resulting in a feedback loop consistent with the operant conditioning theory of negative reinforcement (105). While the expose-recover model is only supported anecdotally in SRC patients, this treatment modality is effective in other populations with anxiety and dizziness (106). As such, further research is warranted to determine the effectiveness of this approach in symptom management for SRC.

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Matching Active Treatments to Each Profile

Determining clinical profiles of concussion (i.e., posttraumatic migraine, vestibular, ocular, anxiety/mood, cognitive/fatigue) is largely dependent on the clinician’s ability to obtain a thorough, multidomain assessment, which includes a biopsychosocial history, injury information, symptom presentation, and clinical examination consisting of evaluations of cognitive, vestibular, and oculomotor function (33).The findings from this multidomain assessment inform more effective and targeted treatment strategies that are individually tailored toward the presenting complaint and increase the likelihood of a successful outcome (7,8). Although behavioral strategies are adequate for rehabilitation and recovery for many athletes following SRC, formal, targeted treatments strategies provided by health care professionals and based on an athlete’s clinical profiles are often warranted.

Each clinical profile requires specific, targeted treatment strategies. For example, patients who are presenting with vestibular dysfunction (i.e., motion/environmental sensitivity, dizziness, lightheadedness, imbalance, vertigo, nausea, and fogginess) following an SRC may find benefit from vestibular therapy to actively rehabituate these systems (31,32). Peripheral vestibular dysfunction (i.e., benign paroxysmal positional vertigo) following concussion also is amenable to targeted vestibular therapies (107). However, in our clinical experience, peripheral vestibular dysfunction affects very few—less than 10% in our clinic—patients following concussion. Ocular complaints following SRC such as blurred or double vision, trouble focusing, convergence or accommodation insufficiencies, or difficulty with pursuits or saccades on oculomotor screening, have shown notable improvement from visual-training exercises (e.g., vision therapy), which are commonly provided through neurovestibular therapy and behavioral optometry (108,109). Given the fairly common emotional and behavioral changes (e.g., anxiety and depression) and the implications that untreated psychiatric issues have on recovery, it is imperative that targeted and adequate treatment is rendered in a timely fashion (56,58). In this regard, psychotherapeutic treatments (i.e., cognitive behavioral therapy and behavioral intervention) have been effective in actively addressing these issues (110,111). Mindfulness-based interventions also have been reported to be effective in reducing postconcussive symptomatology (112,113). In some instances, psychopharmacological intervention may be warranted for persisting and treatment-resistant emotional concerns. In these cases, it is recommended that the patient is referred for a formal psychiatric evaluation to determine the appropriateness of medications in this regard (56). Exertion-based therapy can be used as an adjunct treatment in conjunction with other established treatments or by itself to help promote recovery and determine symptom tolerance with exercise (114,115). Increasing one’s physical exercise also has been shown to improve postconcussive emotional difficulties (75) and in some cases migraine symptoms that mimic those seen following concussion (116,117). Although there is growing support among researchers and clinicians that active, targeted treatments can be effective following SRC and enhance recovery, optimal timing and dose of treatments for SRC have yet to be determined. Future research focusing on the type, timing, frequency, and intensity of specific interventions for athletes with different clinical profiles following SRC is warranted.

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Conclusions

Concussion is heterogeneous and can be conceptualized using a clinical profiles model that includes cognitive/fatigue, vestibular, ocular, migraine, and anxiety/mood profiles. Such an approach can inform more effective management and treatment strategies for athletes with this injury. Sports medicine professionals also should consider modifying factors such as sleep and cervical involvement when evaluating and treating athletes with SRC. Concussion clinical profiles should be informed by a comprehensive approach to assessment that includes clinical interview and examination, medical history (including risk factors) and injury information, concussion symptoms (somatic, cognitive, affective, sleep), and evaluations of impairment (balance, cognitive, ocular, vestibular). Preliminary evidence suggests that the migraine and anxiety/mood primary clinical profiles each represent approximately one quarter of all patients. In addition, vestibular and ocular primary clinical profiles combined represent one third of patients and highlight the importance of assessing vestibular and ocular symptoms and impairment in athletes following SRC. Evidence also indicates that certain primary clinical profiles are associated with specific secondary profiles. For example, the migraine primary clinical profile is associated with an increased likelihood for a secondary vestibular clinical profile. This finding suggests that sports medicine professionals should anticipate these associated profiles in their assessment approach and treatment plan for athletes with SRC. Finally, clinical concussion care is moving toward more active treatments targeted to each specific clinical profile. Moving forward researchers need to continue to examine empirically the clinical profiles-based approach to assessing and treating concussion presented in this paper.

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