A Primer on Concussions in Soccer : The Negligence of FIFA Regarding Head Injuries

In this article I'll examine briefly what a concussion is, the prevalence of concussion in the sport of soccer, and also discuss three incidents of head injury that occurred during this past FIFA World Cup.

WHAT IS A CONCUSSION

Mild traumatic brain injury (mTBI), or concussion, is the most common type of traumatic brain injury/ While typically not too serious in most cases, concussion has a serious risk of short and long-term sequelae. At the 4th International Conference on Concussion in Sport (Zurich, November 2012), a panel discussion took place to obtain a consensus-based definition of a concussion. The Concussion in Sport Group (CISG) defined a concussion as follows:

Concussion is a brain injury and is defined as a complex pathophysiological process affecting the brain, induced by biomechanical forces. Several common features that incorporate clinical, pathologic and biomechanical injury constructs that may be utilised in defining the nature of a concussive head injury include:

In essence, a concussion is a head injury with a temporary loss of brain function that may result in a variety of physical, cognitive, and emotional symptoms. Presently, concussion is a clinical diagnosis based largely on the observed injury mechanism (point of contact, force on head area, etc.), signs, and symptoms. The first step towards a diagnosis of a concussion is actual recognition of the injury.

The hallmark signs and symptoms of acute sports concussion include (but are not limited to):

• Loss of consciousness (LOC) 
• However, the majority of concussions in sports occur without a LOC
• Problems with attentional mechanisms 
• Manifested as (but not limited to): slowness to answer questions and follow directions, easily distracted, poor concentration, vacant stare/glassy eyed.
• Memory disturbance
• Balance disturbance 

These symptoms may be apparent immediately after the head injury or other signs and symptoms of a concussion may evolve and appear gradually over several minutes. Additionally, over the course of the first 24 hours following a concussion injury, other signs and symptoms may manifest. However, it's important to note that there is a large range of these symptoms and they often vary, not all of these symptoms are seen in every case of sports concussion. The most common symptoms reported in concussion literature include:

• Somatic symptoms such as headache
• Cognitive symptoms such as feeling like in a fog
• Emotional symptoms such as lability
• Physical symptoms such as LOC and amnesia
• Behavior changes such as irritability
• Cognitive impairment
• Sleep disturbance (insomnia)
• Dizziness and balance problems
• Blurred vision
• Fatigue

If any one or more of these symptoms is recognized, a concussion should be suspected and a management plan should be implemented.

I'd like to focus on amnesia because it will come into play later. Amnesia is a common physical symptom associated with mTBI. Amnesia almost always involves loss of memory for the traumatic event but frequently includes loss of recall for events immediately before (retrograde amnesia) and after (anterograde amnesia) the traumatic event.

Since concussions are often hard to recognize and to diagnose, the Zurich Consensus on Concussion in Sport proposed diagnostic criteria for sideline evaluation. An athlete shows any of the following, they need to be removed from play and assessed.

• Initial obvious physical signs consistent with concussion (LOC, balance problems)
• Teammates, trainers, coaches observe cognitive or behavior changes in functioning consistent with concussion symptoms reported
• Any concussion symptoms reported by the athlete injured
• Abnormal neurocognitive or balance examination

Following a removal from play:

• Physician evaluated the player using standard emergency management principles, most notably to exclude  severe head trauma or cervical spine injury
• Once first aid issues are addressed, assessment of the concussive injury should be made using the SCAT3 or other sideline assessment tools (NHL uses ImPACT concussion testing, read here: http://www.impacttest.com/about/)
• The player should not be left alone following the injury and serial monitoring for deterioration is essential over the initial few hours following injury
• A player with diagnosed concussion should not be allowed to return to play on the same day. 
• It has been unanimously agreed that an athlete should not return to play on the same day of the injury. Studies have shown that athletes allowed back into play following a concussion may demonstrate neuropsychological deficits post injury. 

CONCUSSION MANAGEMENT AND RECOVERY

The graduated return to play protocol following a concussion is a stepwise process and is outline below: 

In this stepwise progression, an athlete only proceeds to the next level if they are asymptomatic at the current level. Each step should take at least 24 hours, making the minimum amount of time to proceed through the full rehabilitation protocol one full week. Athletes should never return to play on the same day as an injury.

CONCUSSIONS IN THE SPORT OF SOCCER

Most people associate concussions with violent/physical sports, specifically American football, hockey and boxing. Of all sports played in the United States, football is the sport associated with the greatest number of traumatic brain injuries, but it also has the largest number of participants.

In the US, soccer is a sport growing in popularity. Between 1982 ad 2008, approximately 7.2 million men and 5.2 million women played soccer at the high school level and an additional 430,000 men and 322,000 women at the college level (Cantu and Mueller).

Recently, a study (Rosenthal et al) was published which analyzed data from High School Reporting Information Online (HS RIO), a national high school sports injury surveillance system. In this system, high schools across the nation with at least 1 certified athletic trainer were invited to participate. The trainers would log into the system and report injuries and athlete-exposures (AE) which was defined as 1 athlete participating in 1 competition or practice. The study used a sample of 100 schools for participation in the concussion rate study and focused on 9 sports: baseball, boys and girls basketball, football, boys and girls soccer, wrestling, softball and girls volleyball. These sports were chosen because data was available from 2005-2006 through 2011-2012.

The study reported the following rates:

"The HS RIO data showed a significant increase in overall concussion rate in the 7-year period of the study. The rates significantly increased in 5 of the 9 sports studied and showed increasing trends in the others. As can be seen from our results, the majority of the rate increase for all sports was observed after the 2008-2009 academic year."

The graphs from the study shown below show total concussion rates for girls and boys sports from 2005-2006 through 2001-2012:

As you can see, the rate of concussions has increased in both boys and girls soccer. However, girls sustain a higher rate of concussions.

Another study (Gessel et al) also used the HSRIO data to survey the injury and drive targeted injury-prevention projects.  The researchers determined that the risk factors for concussion in soccer differed significantly by sex. Concussions in soccer players most frequently occur as a result of head to head collisions in the act of heading the ball; 40.5% of the time in males and 36.7% in females. Girls soccer players sustain a greater proportion of concussions related to contact to the ground (22% compared to 6%) and contact with the ball (18.3% compared to 8.2%). Another risk factor for concussions in soccer is playing the position of keeper, with 21.7% of injuries to goalkeepers being concussions, compared with 11.1% of injuries to other positions.

Up to 50% of players admit to bending the truth about their symptoms to get back into action more quickly. It's imperative to teach them that a brain injury is not like any others, it could be irreversible. You can cause serious damage by not being honest about your symptoms and condition and by returning to play with a brain injury.

There are three incidents that occurred to three separate players and national teams during the FIFA World Cup that I'd like to discuss.

Progress and Significance of Current Concussion Research - Developing a Blood Biomarker for Brain Injury

If you read my post on Concussions in the NHL, you'll know that a concussion is considered to be among the most complex injuries to diagnose in sports medicine. A concussion is a clinical diagnosis based largely on the observed injury mechanism (point of contact, force on head area, etc.), signs, and symptoms. Due to the fact that there is no true [perfect] diagnostic test for a concussion, physicians must rely on patient-reported symptoms and neurological testing to make a diagnosis. Additionally, unlike other neurological injuries, most concussions cannot be identified by advanced neuroimaging techniques such as CT scans or MRIs.

In this post I'll highlight some current research on concussion.

WHAT WE KNOW

Concussion is still an injury that is largely debated. Most debate surrounds the long-term effects of the injury. What isn't debated is that a player suffering from a concussion should never return to play (RTP) the same day as the injury and should take a minimum of a few days off to recover and rest. Concussion in athletes practicing contact sports is a growing problem worldwide and new research has highlighted some important facts about the injury:

• The underlying pathophysiology of a concussion is an acute disturbance of neuronal function combined with damage to neuronal and glial (neuronal support) cells. This acute disturbance may eventually present chronic consequences (Blennow et al.). 
• Most concussions resolve after 7 days or within a couple weeks; however studies have revealed that 10-15% of concussions remain symptomatic more than a year after the injury. The chronic and sometimes even progressive symptoms of concussion have been linked to repeated injury occurring before the brain has properly recovered (Baugh et al.).
• Cerebrospinal fluid (CSF) can show biochemical changes in the central nervous system (CNS). CSF biomarkers such as total tau (T-tau) and neurofilament light (NFL), show elevated levels of axonal damage after acute damage to the brain (Hesse et al. and Nylen et al.) 
• The levels of these biomarkers correlate with the severity of the brain damage and eventually return to normal after a period of rest (Zetterberg et al. Neselius et al.).
• CSF is obtained via a lumbar puncture, a sometimes painful procedure that is invasive and not optimal for routine testing.

A simple biomarker for concussion which can be used routinely and accurately as a diagnostic tool would be extremely useful for team physicians. This test could not only help diagnose a concussion, but also be useful in follow-up for concussed athletes and aid RTP decisions.

A recent study published in the JAMA Neurology Journal had the objective of "determining if sports-related concussion is associated with elevated levels of blood biochemical markers of injury..." The researchers collaborated with the Swedish Hockey League to conduct the research. 

THE STUDY

DESIGN

In the study Blood Biomarkers for Brain Injury in Concussed Professional Ice Hockey Players, Dr. Pashtun Shahim et al. researched an objective biomarker to help in clinical decisions regarding concussion. The study examined three biomarkers to determine their significance: 

• Neuron-specific enolase (NSE) - a biomarker for neuronal injury (elevated levels found in boxers that had been repeatedly hit in the head (Zetterberg et al).
• S-100B - a glial cell biomarker named S-100 calcium-binding protein B, elevated levels found in boxers who took head shots compared with boxers who only took body shots (Graham et al.).
• Plasma T-tau - elevated levels found in Olympic boxers, which then normalized after rest (Neselius et al.).

The research was approved by the Swedish Ice Hockey Association and ran through the University of Gothenburg. With player's consents, team physicians of all 12 teams in the Swedish Hockey League would collect pre-season data, asking all players to take the Standardized Assessment of Concussion. Two of the consenting teams, Frölunda and Lülea, collected baseline blood samples from all their players prior to the start of the season. 

The study asked physicians to document signs and symptoms of concussion as well as any other examination findings when making their diagnosis. For players who suffered a concussion during the season, blood samples were collected at 1, 12, 36, 48, and 144 hours post-injury (or when the player returned to full-contact). 

RESULTS

Of the 288 players in the SHL, 35 had a sports-related concussion for the duration of the study. 28 of these players' samples were used in data analysis, as the remaining 7 players either withdrew consent or had an uncertain diagnosis. Of these 28 concussions,

• Three (10.7%) suffered a loss of consciousness (LOC)
• 25 (89%) experienced symptoms such as headaches, confusion, dizziness, or nausea. 
• 15 (53.5%) had symptoms lasting longer than 6 days.

T-tau levels were significantly higher in post-concussion samples compared with the pre-season samples. Unfortunately, the S-100B and NSE post-concussion samples were not significantly different from the pre-season samples. However, the samples collected immediately after injury (1 hour) showed elevated levels of both T-tau and S-100B when compared with the pre-season samples. The levels of these two biomarkers peaked at this timepoint (1 hour post-concussion). The levels of T-tau 144 hours after injury remained significantly elevated when compared to baseline samples; however, this did not occur in S-100B and NSE samples.

Assessing the severity of a concussion is important in the management of the injury and determination of when to RTP. The level of T-tau was not significantly different post-concussion for different grades of concussion; however, players whose concussions had symptoms for > 10 days or experienced a LOC had some higher levels. The levels of S-100B 1 hour post-concussion were significantly higher in players that experienced a LOC and those players that had symptoms for > 10 days when compared to players whose symptoms resolved in 6 days.


CONCLUSION
The T-tau biomarker displayed a significant diagnostic accuracy level, where T-tau concentrations at 1 hour post-concussion could accurately predict the number of days it took for concussion symptoms to resolve and the players to experience a safe RTP. Plasma T-tau, while highly specific to the Central Nervous System (CNS), is a promising biomarker which can be used in the diagnosis of a concussion and RTP decisions.

The NHL and NHLPA should consider participating in more studies with researchers. The wealth of information that could be learned from just basic investigation on a few blood samples is highly valuable and could not only aid current players experiencing concussion but also help determine the NHL's future plan for limiting injury.


Sources:

1. Baugh CM, Stamm JM, Riley DO, et al. Chronic traumatic encephalopathy; neurodegeneration following repetitive concussive and subconcussive brain trauma. Brain imaging Behav. 2012;6(2): 244-254. 
2. Blennow K, Hardy J, Zetterberg H. The neuropathology and neurobiology of traumatic brain injury. Neuron. 2012;6(5);886-899. 
3. Hesse C, Rosengren L, Vanmechelen E, et al. Cerebrospinal fluid markers for Alzheimer's disease evaluated after acute ischemic stroke. J Alzheimers Dis. 2000;2(3-4): 199-206. 
4. Nylen K, Csajbok LZ, Ost M, et al. CSF-neurofilament correlates with outcome after aneurysmal subarachnoid hemorrhage. Neurosci Lett. 2006; 404(1-2); 132-136. 
5. Zetterberg H, Hietala MA, Jonsson M, et al. Neurochemical aftermath of amateur boxing. Arch Neurol. 2006;63(9): 1277-1280. 
6. Neselius S, BRisby H, Theodorsson A, Blennow K, Zetterberg H, Marcusson K. CSF-biomarkers in Olympic boxing; diagnosis and effects of repetitive head trauma. PLoS One. 2012;7(4):e33606. 
7. Zetterberg H, Tanriverdi F, Unluhizarci K, Selcuklu A, Kelestimur F, Blennow K. Sustained release of neuron-specific enolase to serum in amateur boxers. Brain Inj. 2009:23(9): 723-726. 
8. Graham MR, Myers T, Evans P, et al. Direct hits to the head during amateur boxing is associated with a rise in serum biomarkers for brain injury. Int J Immunopathal Pharmacol. 2011;24(1): 119-125. 
9. Neselius S, Zetterberg H, Blennow K, et al. Olympic boxing is associated with elevated levels of the neuronal protein tau in plasma. Brain Inj. 2013;27(4): 425-433.