Topic: The Neuro-Ophthalmology of Concussion
By: Leonard Messner, OD, FAAO & Danielle Leong, OD
Abstract:
Sports-related concussion has received increasing attention as a result of short- and long-term neurologic sequelae
seen among athletes. This course gives an overview of the neuro-ophthalmology of concussion, diagnostic testing
and insights into optometry's role in managing concussion.
Learning Objectives:
At the completion of this lecture participants will be able to:
*describe what a concussion is
*describe signs and symptoms of a concussion
*describe the short- & long-term consequences of concussion
*differentiate between remove from play and return to play
*describe concussion prevention strategies
1.
2.
Introduction
a. Case example: 22 year old female soccer player
i. Symptoms: dizziness after bumping heads while heading a ball, no loss of consciousness
ii. History: 2 prior concussions
iii. Exam: Normal neurological examination, orientation, memory, concentration, balance
b. Questions:
i. Did the patient have a concussion?
ii. Do you need to lose consciousness?
iii. Are women more vulnerable than men?
iv. Is there an objective measure for concussion?
v. Should she stop contact sports?
Concussion basics
a. What is a concussion? (McCrory, 2008)
Concussion is defined as a complex pathophysiological process affecting the brain, induced by
traumatic biomechanical forces.
i. Concussion may be caused by a direct blow to the head, face, neck or elsewhere on the
body with an “impulsive” force transmitted to the head.
ii. Concussion typically results in the rapid onset of short-lived impairment of neurologic
function that resolves spontaneously.
iii. Concussion may result in neuropathologic changes but the acute clinical symptoms
largely reflect a functional disturbance rather than a structural injury.
iv. Concussion results in a graded set of clinical symptoms that may or may not involve loss
of consciousness. Resolution of the clinical and cognitive symptoms typically follows a
sequential course however it is important to note that in a small percentage of cases, postconcussive symptoms may be prolonged.
v. No abnormality on standard structural neuroimaging studies is seen in concussion
b. Epidemiology:
i. 1.6 to 3.8 million annually (Thurman et al., 1998; Guskiewicz et al., 2000; Langlois et al.,
2006; American College of Sports Medicine 2006; Guskiewicz et al., 2003; Collins et
al., 2003; Mitka 2010)
ii. An estimated 85% undiagnosed (American College of Sports Medicine, 2006)
iii. Boy's football & Girls soccer highest rates (Halstead & Walter, 2010; Meehan et al.,
2011)
c. National attention of sports concussions
i. Lystedt Law (Washington State Legislature, 2009)
1. Athletes, parents and coaches must be educated about the dangers of
concussions each year.
2.
d.
e.
f.
g.
If a young athlete is suspected of having a concussion, he/she must be
removed from a game or practice and not be permitted to return to play.
When in doubt, sit them out.
3. A licensed health care professional must clear the young athlete to return to
play in the subsequent days or weeks.
ii. Currently 44 of 50 states have enacted concussion laws similar to the Lystedt Law
(Toporek, 2012)
Biomechanics of concussion (Meaney & Smith, 2011; Maruta et al, 2010)
i. Contact force
1. Brain experiences accelerations at the moment of impact (Meaney & Smith,
2011; Maruta et al, 2010)
a. Linear accelerations: Cause increased pressure throughout the brain
leading to neurologic dysfunction
i. Direct & indirect injury (coup & contrecoup)
b. Rotational accelerations: cause shear-induced tissue damage &
stretching of axons
ii. Wash-over effect in blast injuries
Risk Factors
i. Age: Children vs. adults
1. Brains still developing, more sensitive to concussion, weak necks,
disproportionate head to body, weak torso, poor equipment, poor language skills
to alert coach to concussion symptoms, poor access to medical resources,
coaches with various levels of training (Kirkwood et al. 2006; Proctor & Cantu,
2000)
ii. Gender: Males vs. Female concussion rates, theories: neck strength, hormonal factors
Concussion rate 1.7 vs. 1.0
(Frommer et al., 2011; Dick, 2009, Zuckerman et al., 2012, Marar et al., 2012)
iii. Sport: (concussion rate) Football>Hockey>Lacrosse (Kirkwood et al., 2006; McCrea et
al., 2003, Marar et al., 2012)
iv. Level of play: youth vs. high school vs. collegiate
1. High school mean linear acceleration: 24g, College: 22g (Broglio et al., 2009;
Broglio et al,. 2012)
Signs & symptoms (US Dept of Health & Human Services CDC, 2012)
i. Sleep: abnormal sleep, difficulty sleeping, excessive sleep
ii. Emotion: irritability, anxiety, depression, extreme emotions
iii. Cognitive: concentration, memory, thinking, processing speed
iv. Physical: headache, vision, nausea, balance, energy level, sensitivity to noise and light
Neurology of concussion
i. Many symptoms not captured by cognitive testing
1. Vision/oculomotor symptoms: photophobia (occipital lobe, brainstem), blurred
vision (frontal, temporal lobes), diplopia and vertigo (brainstem, cerebellar
paths) (Heitger et al, 2002; Heitger et al, 2010)
2. Anterior corona radiate (dorso-lateral prefrontal cortex, DLPFC) & corpus
callosum (genu) most frequently damaged white matter tracts in mTBI
determined by DTI (Maruta et al, 2010)
a. Gaze tracking error variability during visual tracking as a useful
screening tool for mTBI.Gaze error variability significantly correlated
with attention and working memory measures in neurocognitive testing
DLPFC (Brodmann Areas 9 and 46) responsible for initiation of
saccades (B-46), plays a mjor role in the decisional processes
governing ocular motor behavior (Pierrot-Deseilligny et al., 2005)
b. Saccadic eye movements are controlled by a cortical network
composed of several oculomotor areas: parietal eye field, frontal eye
field, supplementary eye field, cingulate eye field, and DLPFC. DLPFC
in the midfrontal gyrus is involved in reflexive saccade inhibition and
visual short-term memory (Gaymard et al., 1998)
3.
4.
5.
ii. Pathophysiology: Neuronal Injury (Meaney & Smith, 2011)
1. Axonal stretching: microtubule and microscopic axonal injury
2. Neuronal injury: biochemical cascade events (Giza & Hovda, 2001)
3. Ionic imbalance: Glutamate, Potassium, Calcium
a. Non-specific depolarization and initiation of action potentials
b. Release of excitatory neurotransmitters
c. Massive efflux of potassium
d. Increased activity of membrane ionic pumps to restore homeostasis
e. Hyperglycolysis to generate more adenosine triphosphate (ATP)
f. Lactate accumulation
g. Calcium influx and sequestration in mitochondria leading to impaired
oxidative metabolism
h. Decreased energy (ATP) production
i. Calpain activation and initiation of apoptosis
4. Neurotransmission disrupted
5. Energy crisis: cerebral blood flow, energy demand
6. Pediatric SRC is primarily a physiologic injury, affecting CBF significantly
(Maugans et al., 2012)
iii. Window of vulnerability
1. Concussion opens a temporal window of brain metabolic imbalance, the closure
of which does not coincide with resolution of clinical symptoms. The recovery
of brain metabolism is not linearly related to time. A second concussive event
prolongs metabolic normalization (Vognozzi et al., 2007)
Sequelae of concussion
a. Complications of concussion (Guskiewicz et al., 2003; Holsinger et al., 2002; Plassman et al.,
2000; Gavett et al. 2011, Meehan & Bachur, 2009, Putukian, 2011)
i. Symptoms
ii. Risk of subsequent concussion
iii. Risk of second impact syndrome
b. Long-term sequelae
i. Prolonged Post-concussion syndrome
1. 225,000 new patients each year show long-term deficits from mild TBI
(approximately equal to the number of patients diagnosed with breast cancer,
multiple sclerosis, and traumatic spinal cord injury) (Mitka et al., 2010)
ii. Cognitive impairment
1. Cognitive impairment in children with TBI, impaired neuroplasticity and brain
development (Scherwath et al., 2011)
iii. Correlation to neuro-degenerative disease (CTE, Alzheimer's, dementia)
1. 20-30% of Alzheimer's patients report history of head trauma vs. 8-10% of
controls (Guskiewicz et al., 2005)
2. CTE: diagnosis, on-going research (McKee et al. 2009)
Concussion Tests: 2 types (Guskiewicz & Broglio, 2011)
a. Remove from play (diagnosis)
b. Return to play (management)
Concussion Diagnosis (Dziemianowicz et al., 2012)
a. Challenges
i. Variable signs & symptoms
ii. Denial of signs & symptoms
iii. Poor education on signs & symptoms
1. Athletic Trainer assessed concussion vs. athlete concussion symptoms
epidemiology
2. Survey: why concussion was not reported
iv. Neurological & radiological studies limited: metabolic vs. structural changes
v. Evaluation & management protocols lacking
vi. Structural vs. Functional damage: diffuse axonal injury, metabolic impairment, cerebral
blood flow perturbations
1.
b.
c.
Concussion is a metabolic rather than a structural abnormality (Vognozzi et al.,
2010; Choe et al., 2012)
Why do we need a rapid sideline test for concussion?
i. Improve outcomes in athletes with concussion
ii. Prevent possible devastating long-term disability
iii. Prevent risk of subsequent concussion
iv. Need an easy objective test since qualified personnel not always available
v. Need evidence based, validated tests
Concussion assessment tools: Remove-From-Play (Meehan et al., 2011)
i. Modified Glasgow Coma Scale (GCS)
1. For moderate to severe TBI, not mild TBI and concussion (McCrory et al.,
2009)
ii. Symptoms checklist (Putukian, 2011; Alla et al., 2009)
1. Subjective, variable
iii. Sport Concussion Assessment Tool 2 (SCAT2)
1. 20mins to complete, requires medical professional, no 'cut-off' score, not
validated, subjective components, unreliable (McCrea et al., 2005; McCrory et
al. 2009)
iv. Head Impact Telemetry System (HITS) (Talavage, 2010)
v. Standardized Assessment of Concussion (SAC) (McCrea et al., 1997; McCrea et al.,
1998)
1. Doesn't assess brainstem or cerebellar function, tester dependent, requires
baseline
vi. Balance Error Scoring System (BESS) (Guskiewicz, 2011)
1. Performance effected by previous injury, subjective
vii. King-Devick Test (K-D)
1. Requires baseline, new test, objective, sideline test, <1minute to administer,
trained administrator (non-medical)
2. Testing eye movements: concussion anatomy overview
a. DLPFC, FEF, PEF, Visual cortex, Caudate nucleus, GP, STN, SNr, SC,
ON
b. Approximately 55% of the brain's circuits are devoted to vision and eye
movements, abnormalities in these areas correlate with long-term
outcomes of concussion (Heitger et al., 2002; Heitger et al., 2010)
3. K-D concussion protocol: Baseline & Post-injury testing
4. Validated studies & evidence based research
a. Boxers & MMA fighters Study: (n=39) (Galetta et al., 2011)
i. learning effects
ii. post-fight K-D scores correlated with post-fight Military
Acute Concussion Evaluation (MACE) scores
iii. worsening of K-D score by >5 sec noted only in subjects with
head trauma
b. Collegiate Cohort Prospective Study: (n=219) (Galetta et al., 2011)
i. Learning effects
ii. Worsening of K-D score by 5.9sec (avg) in concussed athletes
iii. Exhaustion trial of basketball team (n=18) after 2 hour
scrimmage showed average improvement of K-D time, K-D
test robust to fatigue.
c. New Zealand Amateur Rugby Pilot study: (n=50) (King et al., 2012)
i. Post-game K-D testing revealed 2 incidental concussions
neither witnessed nor reported during the game
d. New Zealand Amateur Rugby Study: (n=37) (King et al., 2013)
i. 5 witnessed concussions, 17 un-witnessed concussions
ii. By incorporating the K-D test as part of the post-match
assessment of players concussive injuries were identified that
may have previously gone unnoticed or unmonitored.
e.
On-Going research:
i. Professional hockey: SCAT2 and K-D
ii. Sports Parents study
iii. Wheaton College
iv. Youth Hockey
Concussion sideline assessment as a composite measure? SAC, BESS, K-D Test
6.
7.
5.
Concussion Management
a. Return to school & Return to play
i. CDC Return to play protocol (McCrory et al, 2008; US Dept of Health & Human
Services CDC, 2012; American Academy of Neurology, 2011)
1. No activity: complete physical, cognitive rest
2. Light aerobic exercise: walking, swimming, stationary bike
3. Sport-specific exercise: running drills in soccer, skating drills in hockey, etc.
4. Non-contact drills: more complex training drills, may start resistance training
5. Full-contact practice: with medical clearance, participate in normal training
activities
6. Return to play: normal game play
ii. Return to School
1. Cognitive rest required to recover from concussion
2. Consider school load: tests, homework, reading
b. Prevention
i. Reduce exposure, reduce hits
1. 75% of head trauma occurs during practice, restrict hitting in practice
ii. The role of helmets (Meaney & Smith, 2011)
1. Helmets originally designed to prevent skull fractures, not concussions. Helmets
can also make the game more dangerous
iii. Education
1. Athletes, coaches, parents, teachers, medical personnel all involved in
management team
a. Up to 40% of concussed athletes return to play prematurely (Yard &
Comstock RD, 2009)
2. Athletes poorly educated on concussions (McCrea et al., 2004)
Conclusions & Questions to be answered
a. Sports related concussion awareness on the rise, increasing incidence with public education
b. Review Case example from intro
c. What are the best tests to diagnose and manage concussions?
d. How can we best develop evidence to support use of current and new tests?
e. In what ways can we lead the effort to reduce effects of concussion?
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