Sport-related concussion (SRC), a subtype of mild traumatic brain injury (mTBI), typically results in reversible neurological dysfunction caused either by a direct blow to the head, neck, or elsewhere on the body with an impulsive force transmitted to the head.1 Sport-related concussion is common in sports medicine, pediatric, and primary-care clinics.2 The first step in establishing the diagnosis in the outpatient setting is a detailed account of the injury and a comprehensive medical history, including a validated concussion symptom questionnaire. Information about symptoms is essential but relying solely on subjective symptom reports is problematic because athletes often under-report symptoms and concussion-related symptoms are nonspecific because they are reported often in patients without concussion.3–5 It is important to document preexisting medical conditions that may impact recovery such as a history of previous concussions, migraine headaches, learning disorders, psychiatric conditions such as depression or anxiety, and preexisting neuro-ophthalmological conditions such as strabismus or convergence insufficiency because they have been associated with prolonged recovery.6 Cognitive function should be assessed using a standardized assessment tool, the most common of which is the Standardized Assessment of Concussion (SAC) of the Sport Concussion Assessment Tool 5 (SCAT5).7 It measures orientation, memory, and concentration.
After the history and cognitive assessment, physicians should perform a focused physical examination (PE) at the initial outpatient visit because physical signs may develop in the 24 hours after injury that were not present at the sideline assessment.1 Recent studies have shown that some physicians who see concussed patients are not current with the latest international recommendations.8 In prior work,9 we presented a comprehensive “toolbox” that contained PE elements that may be useful for the evaluation of concussed patients. In this article, we present directions on how to perform a brief, focused PE to help clinicians efficiently identify physical impairments and track recovery after SRC. Derivation of the Buffalo Concussion Physical Examination (BCPE) is presented in an associated article in this journal. Objective signs, when combined with symptoms, cognitive evaluation and, where indicated, supplementary tests, may help the clinician diagnose concussion and understand the cause of symptoms to prescribe specific treatment for those with prolonged recovery. Acutely concussed patients should in general be seen every 1 to 2 weeks to monitor recovery. If they develop persistent postconcussive symptoms (PPCS), defined as symptoms persisting more than 2 weeks in adults or more than 1 month in children and adolescents,1 the frequency may be subsequently reduced. Primary-care physicians might also consider referring those with PPCS to a multidisciplinary concussion clinic or expert.
Although we are not able to classify all concussed patients into specific categories or subtypes because concussion is a unique injury to each individual patient with several associated conditions, it is useful for the clinician to try to identify the predominant physical signs and symptoms to direct specific treatments for those with PPCS (Figure 1). These classifications may overlap as it is possible to have one or more associated conditions after a head injury.6 Physiological postconcussion syndrome (PCS) is believed to be characterized by persistent autonomic dysfunction and altered control of cerebral blood flow from the global cerebral metabolic disturbance after concussion. These patients typically present with minimal PE abnormalities but can have signs of oculomotor and/or vestibular dysfunction. They often complain of cognitive fatigue and report symptoms with orthostatic vital signs and have early exercise intolerance on graded treadmill testing (ie, symptom-limited exercise at <70% of age-predicted maximum heart rate, HR). Other subclassifications (or associated conditions) include vestibulo-ocular posttraumatic disorder (PTD) and cervicogenic PTD, which present with predominantly vestibulo-ocular and cervical signs and symptoms, respectively. These disorders are not labeled PCS because they are not considered to represent the global metabolic disturbance of brain function after concussion but rather persistent injuries to the central oculomotor and vestibular systems and/or to the upper cervical spine. These patients may demonstrate exercise intolerance during graded treadmill testing but symptom exacerbation typically occurs at a significantly greater workload (beyond 70% of age-predicted maximum HR) than in autonomic/physiological PCS. Some patients with PPCS primarily have affective and/or cognitive symptoms, the management of which is challenging because of the extensive overlap between their symptoms and primary mood disorders. In the authors' experience, PPCS patients whose symptoms are primarily affective and/or cognitive evolve to having minimal PE signs and are capable of exercising to exhaustion during graded treadmill tests without symptom exacerbation. They require a multidisciplinary team approach to treatment that may involve a psychiatrist, a psychologist, and/or a neuropsychologist.
A concussion-specific PE should include evaluation of orthostatic vital signs, cranial nerves, and the oculomotor/ophthalmologic, cervical, and vestibular systems. A sample assessment form of the brief BCPE with directions on how to perform it is presented in the Supplemental Digital Content 1 (see Table, http://links.lww.com/JSM/A200). After orthostatic vital signs have been measured, the BCPE takes about 5 minutes to perform, is recommended for clinicians in the outpatient setting, and is convenient enough to perform at every visit.
Orthostatic Vital Signs
Autonomic dysregulation is common after a head injury and may present with symptoms of orthostatic hypotension (OH), dizziness or vestibular dysfunction, postural orthostatic tachycardia syndrome, or altered HR and blood pressure (BP) responses at rest and during exercise.9 According to the American Autonomic Society, OH is defined as a 20 mm Hg or greater reduction in systolic BP or a >10 mm Hg reduction in diastolic BP after 1 and 3 minutes of standing from the supine position.10 Because the prevalence of OH is between 5% and 30% in the nonconcussed population, this change in BP is clinically significant only when it is accompanied by symptoms of dizziness or lightheadedness.11 Patients with symptoms on standing may have orthostasis and/or a central vestibular injury. Heart rate response is useful because a rise in HR (>40 beats per minute standing vs supine) with a drop in BP usually indicates hypovolemia, whereas lack of HR response is more consistent with a central neurogenic cause. Patients with symptoms of dizziness or vertigo while supine are more likely to have a peripheral vestibular injury and testing including the Dix–Hallpike maneuver or otoscopic examination may be indicated. Orthostatic vital signs are measured only supine to standing because two-thirds of cases can be missed seated to standing.12 Common sources of error for measuring BP include not maintaining the arm at the level of the heart, using an improperly sized cuff, and rapid cuff deflation in those with a slow HR. To save time in clinical practice, orthostatic vital signs can be measured by an allied health professional before seeing the physician follow the BCPE form (see Table, Supplemental Digital Content 1, http://links.lww.com/JSM/A200).
Cranial Nerve Examination
Isolated abnormalities may suggest a brainstem lesion and should prompt further investigation. This part of the PE contains those nerves not assessed during the oculomotor portion of the examination and should always be performed in the first clinical visit. It can be omitted in subsequent visits if no abnormality is found (see Table, Supplemental Digital Content 1, http://links.lww.com/JSM/A200).
Fundoscopy should be performed at the first visit using a standard ophthalmoscope to assess abnormalities in the retina. Abnormal results should prompt further imaging. Abnormal smooth pursuits, repetitive saccades, vestibulo-ocular reflex, near-point convergence (NPC, binocular vision), and abnormal accommodation (monocular vision) are present in up to 69% of adolescents after mTBI.13 Persistent dysfunction may warrant examination by a neuro-ophthalmologist and/or imaging (if not previously performed) because it may represent lesions in cranial nerves, their nuclei, or the brainstem.14 Abnormal and/or symptomatic repetitive saccades and smooth pursuits (complaints of blurred vision, headache, and dizziness) are commonly observed after concussion and may be associated with prolonged recovery.15 Performance of these tests accurately requires experience because they involve observing subtle changes. Quantitative tests such as NPC and accommodation should be performed using a standard accommodation rule (Figure 2). The patient is instructed specifically to report diplopia for NPC and blurred vision for accommodation testing. Due to age-related changes in the eye, normal NPC values are lower in children (diplopia reported >6 cm from the forehead) than in adults (diplopia reported >10 cm from the forehead).16 Follow the BCPE form (see Table, Supplemental Digital Content 1, http://links.lww.com/JSM/A200).
The neck and suboccipital regions are frequently involved in head injuries and can cause headaches, persistent dizziness, and balance difficulties.17 Immediately after the injury, the cervical spine should be assessed and managed if needed. In the outpatient setting, typically a few days after the injury, subacute neck injuries can closely mimic the symptoms of concussion.17 There may be transient mild symptom exacerbation late in systematic exertion testing but the patient can typically exercise to near maximum for age and fitness level. This pattern distinguishes cervical injury from the early and significant symptom exacerbation that causes patients with physiological PCS to terminate exercise early during systematic exercise assessment. Follow the BCPE form (see Table, Supplemental Digital Content 1, http://links.lww.com/JSM/A200).
Postural control and motor coordination problems are common after concussion and could lead to further injuries during sport or work.18 Objective signs of vestibular pathology may not be detectable at rest but only on provocation, potentially pointing to subtle vestibular pathology.15 The Balance Error Scoring System (BESS) test and the modified BESS are validated tests that are typically used to assess balance on the sideline. For clinicians in a busy clinic, tandem gait and tandem stance are more useful tests because of their convenience and high interrater reliability.19 Dual-task tandem gait tests (for example, reciting the months of the year in reverse during tandem gait) may be more sensitive for unmasking subtle vestibular problems after concussion. Follow the BCPE form (see Table, Supplemental Digital Content 1, http://links.lww.com/JSM/A200).
Sometimes the clinician is not sure whether the symptoms are due to concussion, or there may be a particularly prominent symptom (eg, a significant memory problem) that warrants additional testing. Exercise tolerance after concussion may be assessed using a graded aerobic treadmill test such as the Buffalo Concussion Treadmill Test (BCTT). The BCTT is particularly useful for assessing the exercise capacity of patients with PPCS but has been shown to be safe even when performed within the first week after SRC in adolescents.20 Early exercise intolerance (test stopped because of symptom exacerbation of headache or dizziness below 70% of age-appropriate maximum HR) at the initial examination is very sensitive for diagnosing physiological concussion, whereas exercise intolerance later in the test (test stopped because of symptom exacerbation or fatigue above 70% of age-appropriate HR maximum) is suggestive of other cause of the symptoms such as cervical injury and/or vestibulo-ocular subsystem dysfunction.21 The HR at symptom exacerbation will improve as the patient recovers; so, classification is based on the initial test. The ability to exercise to maximum without symptom exacerbation and patient report of a baseline level of symptoms at rest correlates with cardiovascular and cerebrovascular physiological recovery from concussion.20 In those patients with significant vestibular complaints or other injuries that prevent them from walking on a treadmill, an equivalent graded aerobic test can also be performed on a stationary bike with adjustable resistance.22 Exercise that rapidly raises HR, for example weightlifting or sprinting, is not recommended for assessing the symptom exacerbation threshold in concussed patients because they cause a rapid increase in cerebral blood flow. Formal neurocognitive tests are a frequently used and convenient method to assess cognitive difficulties after concussion.23 The use of formal neurocognitive testing (computerized or paper/pencil) for monitoring recovery is not always recommended but should be considered if the patient complains of persistent concentration deficits or a significant deficit was documented during the SAC.7 These patients should be monitored longitudinally until return to baseline (or age-appropriate norm if baseline is not available).
This brief concussion PE combines elements of the SCAT5 and the Vestibular/Ocular Motor Screening (VOMS)15 test while adding greater emphasis to assessing autonomic function, dynamic balance, and the cervical spine. It is recommended for the outpatient setting and not for sideline use. The BCPE was designed to be used in adolescents and young adults and may therefore not be useful for younger children or older adults. A PE is dependent on physician skill; so, this examination requires practice. Subtle signs such as abnormal saccadic eye movements, for example, may be missed and have poor interrater reliability.24 Orthostatic hypotension guidelines recommend measuring BP after 1 and 3 minutes of standing, whereas we measured it only after 1 minute of standing. The baroreceptor reflex requires only a few seconds to stabilize BP in a healthy state; so, we assumed that the majority of healthy participants would normalize at the 1-minute time point. Furthermore, performing a 3-minute measurement does not have much clinical utility because it is not routinely performed in the outpatient setting. Finally, this focused PE should not be used in isolation but in combination with a comprehensive history, a cognitive evaluation, and supplementary tests when indicated.
This article presents a brief, pertinent, and practical PE for concussed patients, the BCPE, that includes orthostatic vital signs and examinations of the cranial nerves, oculomotor/ophthalmologic, cervical, and vestibular systems. It is recommended that a PE be performed at the initial visit and every 1 to 2 weeks after SRC. It is important for clinicians to perform a pertinent PE in patients after concussion to help to establish the diagnosis, define recovery, and to identify potential treatment targets in patients with persistent symptoms.
1. McCrory P, Meeuwisse W, Dvorak J, et al. Consensus statement on concussion
in sport—the 5th International Conference on Concussion
in Sport held in Berlin, October 2016. Br J Sports Med. 2017;51:838–847.
2. Arbogast KB, Curry AE, Pfeiffer MR, et al. Point of health care entry for youth with concussion
within a large pediatric care network. JAMA Pediatr. 2016;170:e160294.
3. Kroshus E, Garnett B, Hawrilenko M, et al. Concussion
under-reporting and pressure from coaches, teammates, fans, and parents. Soc Sci Med. 2015;134:66–75.
4. Hunt AW, Paniccia M, Reed N, et al. Concussion
-like symptoms in child and youth athletes at baseline: what is “typical”? J athletic Train. 2016;51:749–757.
5. Alla S, Sullivan SJ, McCrory P. Defining asymptomatic status following sports concussion
: fact or fallacy?. Br J Sports Med. 2012;46:562–569.
6. Ellis MJ, Leddy JJ, Willer B. Physiological, vestibulo-ocular and cervicogenic post-concussion
disorders: an evidence-based classification system with directions for treatment. Brain Inj. 2015;29:238–248.
7. Echemendia RJ, Meeuwisse W, McCrory P, et al. The sport concussion
assessment tool 5th edition (SCAT5). Br J Sports Med. 2017;51:848–850.
8. Haider MN, Leddy JJ, Baker JG, et al. Concussion management
knowledge among residents and students and how to improve it. Concussion
9. Matuszak JM, McVige J, McPherson J, et al. A practical concussion
physical examination toolbox evidence-based physical examination for concussion
. Sports Health. 2016;8:260–269.
10. Freeman R, Wieling W, Axelrod FB, et al. Consensus statement on the definition of orthostatic hypotension, neurally mediated syncope and the postural tachycardia syndrome. Clin Auton Res. 2011;21:69–72.
11. Low PA. Prevalence of orthostatic hypotension. Clin Auton Res. 2008;18:8–13.
12. Cooke J, Carew S, O'connor M, et al. Sitting and standing blood pressure measurements are not accurate for the diagnosis of orthostatic hypotension. QJM. 2009;102:335–339.
13. Master CL, Scheiman M, Gallaway M, et al. Vision diagnoses are common after concussion
in adolescents. Clin Pediatr. 2016;55:260–267.
14. Shawkat FS, Kriss A, Thompson D, et al. Vertical or asymmetric nystagmus need not imply neurological disease. Br J Ophthalmol. 2000;84:175–180.
15. Anzalone AJ, Blueitt D, Case T, et al. A positive vestibular/ocular motor screening (VOMS) is associated with increased recovery time after sports-related concussion
in youth and adolescent athletes. Am J Sports Med. 2017;45:474–479.
16. Ostadimoghaddam H, Hashemi H, Nabovati P, et al. The distribution of near point of convergence and its association with age, gender and refractive error: a population‐based study. Clin Exp Optom. 2017;100:255–259.
17. Marshall CM, Vernon H, Leddy JJ, et al. The role of the cervical spine in post-concussion
syndrome. Phys Sportsmed. 2015;43:274–284.
18. Kontos AP, Elbin R, Schatz P, et al. A revised factor structure for the post-concussion
symptom scale: baseline and postconcussion factors. Am J Sports Med. 2012;40:2375–2384.
19. Schneiders AG, Sullivan SJ, Gray AR, et al. Normative values for three clinical measures of motor performance used in the neurological assessment of sports concussion
. J Sci Med Sport. 2010;13:196–201.
20. Leddy JJ, Hinds AL, Miecznikowski J, et al. Safety and prognostic utility of provocative exercise testing in acutely concussed adolescents: a randomized trial. Clin J Sport Med. 2018;28:13–20.
21. Leddy JJ, Kozlowski K, Donnelly JP, et al. A preliminary study of subsymptom threshold exercise training for refractory post-concussion
syndrome. Clin J Sport Med. 2010;20:21–27.
22. Leddy JJ, Haider MN, Ellis M, et al. Exercise is medicine for concussion
. Curr Sports Med Rep. 2018;17:262–270.
23. Haider MN, Leddy JJ, Pavlesen S, et al. A systematic review of criteria used to define recovery from sport-related concussion
in youth athletes. Br J Sports Med. 2018;52(18);1179–1190.
24. Maples W, Ficklin T. Interrater and test-retest reliability of pursuits and saccades. J Am Optometric Assoc. 1988;59:549–552.