Evaluation and management of concussion involves many factors, some of which may predict the potential for prolonged or persistent post-concussion symptoms and long-term health effects.
The current international consensus of concussion experts ("Zurich consensus statement") (1) is that a range of "'modifying' factors may influence the investigation and management of concussion, and, in some cases, may predict the potential for prolonged or persistent symptoms, and in others suggest consideration be given to retirement [1] from contact or collision sports:
Factors | Modifier |
Symptoms [2] |
Number [3] (6) [3]Duration (greater than 10 days) Severity [4] (7) |
Signs [2] |
Prolonged loss of consciousness (more than 1 minute duration) [5] Amnesia [6] (Note that amnesia was not found in two 2013 studies (6,7) to be predictive of longer recovery, adding to an already muddled picture as to the role amnesia plays in predicting concussion recovery) |
Sequelae | Concussive convulsions (Note: it is puzzling that impact seizures are still listed as a modifying factor, as a study published simultaneously with the Zurich consensus statement (9) catagorically states that "the literature does not suppport the inclusion of impact seizures as a concussion modifer." |
Temporal |
Frequency - repeated concussions [7] over time (as discussed in the literature review accompanying the Zurich statement (9) @ Table 2, citing studies @ notes 31,103, 34, 17, and 12, "in general, athletes with a previous history of concussion are more likely to present a longer duration of symptoms and are withdrawn from competition for longer following their injury." While multiple concussion history was not found to be predictive of concussion symptoms lasting more than 28 days in one 2013 study [8] (7), another 2013 study [9](14) found that concussion symptoms lasted twice as long for patients with a history of previous concussion as those without such a history (24 versus 12 days); that the median symptom duration for those with a multiple concussion history and who had sustained a concussion within the past year was 2 and 1/2 times longer (28 days) and nearly three times (33 days) longer respectively, compared with patients without such risk factors. Timing - injuries close together in time (14) "Recency" - recent concussion or traumatic brain injury (TBI) [Note: timing and recency continue to be included in the list of modifying factors despite the finding in the accompanying literature review (9) that there is "limited evidence to suggest that the timing or 'recency' makes any difference to timeframe of recovery following a concussion." A subsequent 2013 study [9] (14), however, suggests that children and adolescents who have sustained a single concussion within the past year are at even greater risk of prolonged symptoms. |
Threshold | Repeated concussions occurring with progressively less impact force or slower recovery after each successive concussion [7] (Note, once again, the literature review accompanying the Zurich statement (9) concludes that the evidence to suggest longer timeframes of recovery for each subsequent concussion is "limited.") |
Age | Children and adolescents (less than 18 years old). "Recovery from concussion in children generally takes longer than that in adults. This is evident in time taken for symptom resolution, as well as neurocognitive recovery." (9) (Note, however, that two 2013 studies (6,7) did not find age to be predictive of symptoms lasting more than a week [3] or more than 28 days or more than 28 days, respectively.) [4] Note: delayed onset [10] of symptoms is more common among younger athletes. |
Co- and pre-morbidities (pre-existing medical conditions) | Migraine [11](11,12), depression or other mental health disorders (11,12), attention deficit hyperactivity disorder (ADHD) [12](13), learning disabilities, sleep disorders. |
Medication | Psychoactive drugs, anticoagulants |
Behavior | Dangerous/more aggressive style of play (may be one reason athletes suffer recurrent concussions (5)) |
Sport | High risk activity, contact and collision sport, high competitive level |
The presence of any of these modifying factors at the time of injury, says the Zurich consensus statement, should alert the treating practitioner -and parents - to the possibility that the recovery period will be longer than the 7 to 10 day period typical of the majority (80-90%) of concussions, or that the concussed athlete may have a poorer long-term prognosis, although, as the discussion above demonstrates, there are no hard-and-fast rules and concussion management continues to be largely a matter of clinical judgment based on individual assessment.
Because of the different physiological response and longer recovery after concussion and specific risks related to head injuries during childhood and adolescence, these modifying factors likely apply even more to kids than adults and may mandate more cautious return to play advice, the Zurich statement says.
Two 2013 studies (6,7), however, found that neither age nor LOC was a risk factor for concussion symptoms lasting more than a week and 28 days respectively, and reported different findings on amnesia as a risk factor, the first finding amnesia to be associated with concussive symptoms ≥1 week only in males, but not females, and the second finding no link between amnesia and concussive symptoms lasting more than a month.
The two studies likewise reported inconsistent findings regarding multiple concussion history as a risk factor: the first finding that it doubled the risk for concussive symptoms ≥1 week, but only in football players, and the second finding no link between multiple concussion history and persistent symptoms.
Another 2013 study (12) found an association between post-traumatic migraines (as opposed to simple headaches, the most common concussion symptom), and cognitive impairments and protracted recovery from concussion.
No wonder, then, that the Zurich consensus statement is careful to qualify its findings about modifying factors, correctly acknowledging that "in some cases, the evidence for their efficacy is limited."
The Zurich consensus statement "accepted that gender may be a risk factor for injury and/or influence injury severity" but did not list female gender as a possible modifier [13] in the management of concussions because there was no "unanimous agreement that the current published research evidence is conclusive enough."
A literature review (9) issued with the Zurich consensus statement noted that, while the data suggested that in sports that use the same rules (soccer (3) and basketball (15)), the reported incidence of concussion is greater in females than their male counterparts, concussion risks between genders were not significant in lacrosse, softball/baseball or gymnastics. (15) The study cited five studies (3,16,17,18, 19,20) to support its finding that "there apppears to be differences in how women experience concussive symptoms as well as how long symptoms persist compared with men."
A 2010 study [14] in the Journal of Athletic Training (2), for instance, contradicted the finding of a 2007 study (3) that girls take much longer than boys for concussion symptoms [2] to resolve and return to play. It found no gender difference in terms of the time it took for symptoms to clear and for high school girls and boys to return to play.
The 2010 study did show, however, that female high school athletes present with different symptoms from male athletes, and because they are more likely to report drowsiness (a neurobehavioral or "sleep" symptom) and sensitivity to noise (a somatic symptom) than males - symptoms which may be more easily missed on a sideline or initial assessment or attributed to other underlying conditions, such as stress, depression, or anxiety - the authors of the study, including Dawn Comstock, who was one of the authors of the 2007 study, recommend that, where such symptoms are reported, they be viewed as symptoms of concussion until pre-existing neurobehavioral conditions are ruled out on more detailed examination.
A 2012 study (4) by researchers at Vanderbilt University found no statistically significant differences between tightly matched, homogeneous groups of concussed male and female high school soccer players, either in terms of symptom score reported at baseline or in the first week after concussive injury, or in terms of postconcussion computerized neurocogntive test scores, with the only significant difference between baseline-to-postconcusson being in the total number of symptoms reported.
The only significant gender-related difference identified by the Vanderbilt researchers was that female high school soccer players reported a greater number of post-concussion symptoms. The trend in the research, however, is to focus on total symptom score, not differences in individual symptoms, said Tracey Covassin PhD., ATC, an Associate Professor and Undergraduate Athletic Training Program Director at Michigan State University, and author of four studies on the subject. (15,16,17, 21, 22)
The reason, said the Vanderbilt researchers, may have been due to the fact that prior studies, "have not routinely and consistently controlled for the potentially confounding variables of age, years of education, specific sport, number of prior concussions, time of testing postinjury, medical history, and other biopsychological moderating variables (for example, medical history, presence of ADHD and/or learning disability and so on)."
While the authors of Vanderbilt study recognized that the "results of this study could well be interpreted to indicate that there is no gender-based difference in acute response to concussive injury in high school athletes," either in terms of symptoms or neurocognitive scores, they neverless viewed the results as "supportive" of the 2009 Zurich consensus statement's position - carried forward in the 2013 Zurich statement, that gender "may be a risk factor for injury and/or influence injury severity" (1), at least for athletes in soccer.
A 2012 study (21) recommends that gender be considered by clinicians when interpreting the results of symptom reports [15], neurocognitive testing [16], and postural instability assessments (e.g. BESS [17]) following concussion. Another 2013 study [4] (7) found that sex was not associated with with prolonged (≥28 days) symptom duration.
Most recently, two studies, published just 10 days apart in November 2013 (22, 23) reported gender differences in the way females respond to concussion.
The first (22) found "partial support" for sex differences in male and female concussed high school soccer players, specifically, that female concussed soccer athletes scored lower on neurocognitive tests of visual memory compared with male concussed soccer athletes at 8 days after concussion, and had a significantly greater number of total postconcussion symptoms than male concussed athletes. The findings were in contrast to those reported in the 2012 Vanderbilt study (4), which did not report any differences in postconcussion neurocognitive measures between male and female high school soccer players. The only difference was that the new study, authored by Michigan State's Covassin (and bringing to four the number of separate studies she has authored on gender and concussions), controlled for BMI (body mass index).
The second (23) found that women injured during the two weeks leading up to their period (the premenstrual phase) had a slower recovery and poorer health one month after injury compared to women injured during the two weeks directly after their period or women taking birth control pills.
The new studies appear to support gender as a modifying factor in the management of concussion, but it remains to be seen whether the next international consensus statement will classify it as such when it is issued in 2017.
Further complicating matters, and illustrating just how little true consensus there is in the evaluation and management of sport-related concussion, the 2013 guidelines issued by the American Academy of Neurology (AAN)(10) depart in a number of respects from the Zurich consensus statement and/or the findings of recent studies. The AAN concludes that:
2. Frommer L, Gurka K, Cross K, Ingersoll C, Comstock R.D., Saliba S. Sex Differences in Concussion Symptoms of High School Athletes. J Ath Tr. 2011; 46(1):000-000.
3. Gessel LM, Fields SK, Collins CL, Dick RW, Comstock RD. Concussions among United States high school and collegiate athletes. J Ath Tr. 2007;42:495-503.
4. Zuckerman SL, Solomon GS, Forbes JA, Haase RF, Sills AK, Lovell MR. Response to acute concussive injury in soccer players: is gender a modifying factor? J Neurosurg: Pediatrics 2012; DOI:10.3171/2012.8.PEDS12139 (published online ahead of print October 2, 2012)(accessed October 15, 2012)
5. McCrory P, Johnston KM, Mohtadi NG, Meeuwisse W. Evidence-based review of sport-related concussion: basic science. Clin J Sport Med 2001;11:160-165.
6. Chrisman SP, Rivara FP, Schiff MA, Zhou C, Comstock R.D. Risk factors for concussive symptoms 1 week or longer in high school athletes. Brain Injury 2013;27(1):1-9.
7. Meehan W, Mannix R, Straccoilini A, Elbin R, Collins M. Symptom Severity Predicts Prolonged Recovery after Sport-Related Concussion, But Age and Amnesia Do Not. J Pediatrics 2013;
8. Lau BC, Kontos AP, Collins MW, Mucha A, Lovell MR. Which On-Field Signs/Symptoms Predict Protracted Recovery From Sport-Related Concussion Among High School Football Players? Am J Sports Med 2011;20(10) DOI:10.1177/0363546511410655 (published June 28, 2011 online ahead of print)(accessed November 5, 2011).
9. Makdissi M, Gavis G, Jordan B, et al. Revisiting the modifiers: how should the evaluation and management of acute concussions differ in specific groups? Br J Sports Med 2013;47:314-320.
10. Giza C, Kutcher J, Ashwal S, et al. Summary of evidence-based guideline update: Evaluation and management of concussion in sports: Report of the Guideline Development Subcommittee of the American Academy of Neurologists. Neurology 2013;DOI:10.1212/WNL.0b013e31828d57dd (published online ahead of print March 18, 2013).
11. Lords Q, Greene JP. Traumatic Migraine Versus Concussion: A Case Report. Sports Health Multidisciplinary App. 2013. DOI:10.1177/19417381139491701 (published online ahead of print June 26, 2013).
12. Kontos AP, Elbin RJ, Lau B, Simensky S, Freund B, French J, Collins MW. Posttraumatic Migraine as a Predictor of Recovery and Cognitive Impairment After Sport-Related Concussion. Am J Sports Med 2013;20(10). DOI:10.1177/0363546513488751 (published online ahead of print May 22, 2013)
13. Bonfield CM, Lam S, Lin Y, Greene S. The impact of attention deficit hyperactivity disorder on recovery from mild traumatic brain injury. J Neurosurg: Pediatrics 2013. DOI:10.3171/2013/5.PEDS12424 (published online ahead of print, June 25, 2013)
14. Eisenberg M, Andrea J, Meehan W, Mannix R. Time Interval Between Concussions and Symptom Duration. Pediatrics 2013;132(1):1-10.
15. Covassin T, Swanik C, Sachs M. Sex differences and the incidence of concussions among college athletes. J Athl Train 2003;38:238-244.
16. Colvin AC, Mullen J, Lovell MR, West RV, Collins MW, Groh M. The Role of Concussion History and Gender in Recovery from Soccer-Related Concussion. Am. J. Sports Med 2009;37(9):1699-1704.
17. Covassin T, Swanik CB, Sachs M, Kendrick Z, Schatz P, Zillmer E, et. al. Sex differences in basesline neuropsychological function and concussion symptoms of concussed collegiate athletes. Br J Sports Med 2006;40:923-927.
18. Broshek DK, Kaushik T, Freeman JR, Erlanger D, Webbe F, Barth JT. Sex differences in outcome following sports-related concussion. J Neurosurg 2005;102:856-863.
19. Dick R. Is there a gender difference in concussion incidence and outcomes? Br J Sports Med 2009;43:146-150.
20. Kutcher J, Eckner J. At-risk populations in sports-related concussin. Curr Sports Med Rep 2010;9:16-20.
21. Covassin T, Elbin R, Harris W, Parker T, Kontos A. The Role of Age and Sex in Symptoms, Neurocognitive Performance, and Postural Stability in Athletes After Concussion. Am J Sports Med 2012;40(6):1303-1312.
22. Covassin T, Elbin RJ, Bleecker A, Lipchik A, Kontos AP. Are There Differences in Neurocognitive Function and Symptoms Between Male and Female Soccer Players After Concussions? Am J Sports Med. 2013;20(10). DOI:10.1177/0363546513509962.
23. Wonderle K, Hoeger KM, Wasserman E, Bazarian JJ. Menstrual Phase as Predictor of Outcome After Mild Traumatic Brain Injury in Women. J Head Trauma Rehabil. 2013;DOI:10.1097/HTR000000000006.
Most recently revised and updated November 21, 2013; most recently reviewed December 4, 2015
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