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‘Subconcussive’ is a dangerous misnomer: hits of greater magnitude than concussive impacts may not cause symptoms
  1. Christopher J Nowinski1,2,
  2. Hye Chang Rhim3,
  3. Ann C McKee1,4,5,
  4. Ross D Zafonte3,6,
  5. David W Dodick7,
  6. Robert C Cantu1,2,8,
  7. Daniel H Daneshvar3,6
  1. 1Boston University Alzheimer’s Disease Research and CTE Centers, Boston University Chobanian & Avedisian School of Medicine, Boston, MA, USA
  2. 2Concussion Legacy Foundation, Boston, MA, USA
  3. 3Department of Physical Medicine and Rehabilitation, Harvard Medical School, Boston, MA, USA
  4. 4Department of Neurology, Boston University Chobanian & Avedisian School of Medicine, Boston, MA, USA
  5. 5Department of Pathology, Boston University Chobanian & Avedisian School of Medicine, Boston, MA, USA
  6. 6Mass General Brigham Spaulding Rehabilitation, Boston, MA, USA
  7. 7Department of Neurology, Mayo Clinic, Rochester, Minnesota, USA
  8. 8Cantu Concussion Center, Emerson Hospital, Concord, MA, USA
  1. Correspondence to Dr Daniel H Daneshvar, Department of Physical Medicine and Rehabilitation, Harvard Medical School, Boston, Massachusetts, USA; ddaneshvar{at}mgh.harvard.edu

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Concussion is a traumatic brain injury (TBI) defined by the presence of transient signs and symptoms related to alterations in brain function due to biomechanical force.1 2 However, not every such force results in acute signs or symptoms, and recent research seeks to better understand the sequelae of both forces and injuries that are subclinical. The term ‘subconcussive’ has emerged to refer to both subclinical head acceleration events (HAEs) and injuries (as defined by clinical, biomarker and/or neuroimaging changes). We believe that this term can be misleading in both instances and should be replaced.

When referring to impacts, the prefix ‘sub’ implies lower magnitude HAEs than those that cause a diagnosed concussion. However, sensor studies show that many HAEs are associated with greater head acceleration than impacts that result in a diagnosed concussion. We suggest replacing subconcussive with the more agnostic term ‘non-concussive’.

When referring to injuries, the term subconcussive is a contradiction. If a concussion is a TBI, a subconcussive event implies no injury occurred. However, impacts that do not result in diagnosed concussions are sometimes associated with evidence of neurological injury, including functional changes that do not meet criteria for concussive symptoms, biomarker changes and structural changes evident on neuroimaging.3 There is increasing evidence that these injuries are associated with long-term sequelae.4 5 Researchers are misusing ‘subconcussive’ when referring to these injuries without overt clinical signs or symptoms. For the reasons detailed below, we suggest replacing subconcussive when referring to injury with ‘subclinical TBI’.

Hits of greater magnitude than concussive HAEs may not cause symptoms

With the arrival of football helmet accelerometers, researchers hoped to identify HAE magnitude thresholds that would characterise concussion. Unfortunately, there is no such threshold. A study of 319 college football players reported that peak linear and rotational accelerations were not correlated with symptom frequency, severity score or any symptom.6 In a study of 283 348 impacts from 185 college football players, Mihalik et al found that the positive predictive value of sensor data for identifying concussion at any threshold was less than 2%, despite conservatively adjusting for undiagnosed injuries.7

While concussions tend to be among the hardest impacts sustained, athletes experience HAEs of greater magnitude that do not appear to cause concussion symptoms. Campolettano et al studied 124 youth football players aged 9–14 and analysed the head acceleration experienced by the 15 diagnosed with concussion. They found that for only three (20%), the concussion occurred on the highest linear or rotational magnitude impact the athlete experienced during the study. On average, concussions occurred at the 93.9 percentile linear impact, and 85.2 percentile rotational impact.8 Similarly, Mihalik et al reported that over 4400 non-concussive impacts occurred with greater linear acceleration than for the median concussion. For each concussion diagnosed, there were approximately 340 non-concussive impacts of greater linear acceleration than the median concussive impact.7

Stemper et al studied 511 college football players who experienced 424 059 head impacts. They sustained 4589 head impacts with greater linear and rotational acceleration than the mean accelerations for concussed athletes, and 249 160 head impacts with greater linear and rotational acceleration than the lowest magnitude concussive impact.9

While the football helmet accelerometers are susceptible to measurement errors and peak linear and rotational acceleration may not best capture concussion risk, these studies highlight that ‘subconcussive’ impacts are frequently associated with greater head acceleration than concussive impacts. The term ‘non-concussive’ better captures this range of impacts and reveals that a meaningful proportion of these impacts are ‘high acceleration non-concussive’. More recently, instrumented mouthguards have been developed to quantify head acceleration, and future studies using these devices may further substantiate this claim.10–12

HAEs without symptoms may result in injury

There is growing evidence that some non-concussive impacts sometimes cause subclinical, or silent, TBI, which may cause occult deficits and disease. Acutely, HAEs without symptoms of concussion have been associated with increasing biomarkers of neuroinflammation, suggesting possible neurological injury.3 Imaging studies have demonstrated that repetitive head impacts in the absence of symptomatic concussion are associated with functional impairment and structural damage to the integrity of brain structures including white matter changes, cortical thinning and volume loss.3 Over time, athletes sustaining non-concussive HAEs may also be at higher risk of concussion.9 13

In the long-term, cumulative exposure to non-concussive impacts may increase the risks of neurodegenerative disease including amyotrophic lateral sclerosis (ALS)5 and chronic traumatic encephalopathy (CTE).4 Duration of exposure to non-concussive HAEs has been described as being higher in professional football players with ALS compared with those without,5 and in predicting both CTE status and severity whereas concussion does not.4

If these HAEs have acute and long-term sequelae, they should be identified as separate from, but not necessarily less than, concussion, as the word ‘subconcussive’ may imply. The observation that some non-concussive impacts can have clinical implications is unsurprising given the widely accepted evidence that subclinical injury can lead to neurological deficits in other disease processes, such as how some ischaemic events can lead to subclinical cerebrovascular disease that can accumulate and eventually manifest as dementia and cognitive decline.14 Introducing a ‘subclinical’ classification to TBI brings TBI in line with other neurological diseases.15

Recommendations

The term ‘subconcussive’ should be retired when referring to both impacts and injuries (table 1). We recommend using ‘non-concussive’ to describe HAEs that do not result in a diagnosed concussion. Research-to-date suggests that while some non-concussive HAEs are harmless, others may cause injury associated with changes in brain function, biomarkers and imaging. The absence of symptoms following an HAE does not indicate that no injury occurred, but rather that no injury occurred to a salient network; it is possible that damage occurred in an area that is not responsible for conscious processes. It is also possible that sensory obtundation has occurred in some individuals exposed to TBI, further weakening the link between TBI and symptoms. In addition, we anticipate there are differences in how individuals respond to the same head impact based on unique differences in brain anatomy, premorbid risk factors and comorbid conditions, which can lead to differences in subsequent injury risk. Moreover, given the wide range of HAE magnitudes and potential negative consequences associated with repetitive concussive and non-concussive HAEs, individual-based metrics considering an athlete’s cumulative impact history are important in preventing subsequent injury and long-term sequelae. By changing the nomenclature, we hope to add specificity and clarity to the growing conversation exploring non-concussive impacts on subclinical TBI and neurological outcomes.

Table 1

Current and proposed impact and injury terminology

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References

Footnotes

  • Contributors All authors participated in conceptualisation, writing original draft and reviewing and editing.

  • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

  • Competing interests CN is the cofounder and chief executive officer of the Concussion Legacy Foundation; reported non-financial support (travel reimbursement) from the NFL Players Association as a member of the Mackey-White Health & Safety Committee, WWE and AEW (All Elite Wrestling); and serves as an advisor and options holder for Oxeia Biopharmaceuticals, PreCon Health and StataDx outside the submitted work. ACM is a member of the Mackey-White Committee of the National Football League Players Association. RZ receives royalties from Oakstone for an educational CD (Physical Medicine and Rehabilitation: A Comprehensive Review) and from demosMedical, part of Springer Publishing, for serving as coeditor of the text Brain Injury Medicine and serves on the Scientific Advisory Board of Oxeia Biopharma, BioDirection, ElMINDA and Myomo. He is also PI on a grant entitled the Football Players Health Study at Harvard University, which is funded by the National Football League Players Association (NFLPA) and evaluates patients for the MGH Brain and Body TRUST Center, sponsored in part by the NFLPA, and serves on the Mackey-White Health and Safety Committee. DWD reports consulting for AYYA Biosciences, Abbvie, Allergan, Amgen, Atria Health, Biohaven, CapiThera, Cerecin, Ceruvia Lifesciences LLC, Cooltech, Ctrl M, Eli Lilly and Co, GSK, Impel, Lundbeck, Nocira, Novartis, Perfood, Pfizer, Praxis, Revance, Satsuma, Theranica and WL Gore; payment or honoraria for lectures/presentations/educational events for Abbvie, Allergan, Amgen, Biohaven, Eli Lilly and Co, Lundbeck, Pfizer, Novartis and Teva. He participates on a data safety monitoring Board or advisory board for Abbvie, Allergan, Amgen, Biohaven, Eli Lilly, Lundbeck and Novartis. He reports honoraria for Academy for Cambridge University Press, Continued Healthcare Learning, Clinical Care Solutions, CME Outfitters, Curry Rockefeller Group, DeepBench, Global Access Meetings, KLJ Associates, Majallin LLC, Medlogix Communications, Miller Medical Communications, MJH Lifesciences, Oxford University Press, Vector Psychometric Group, WebMD Health/Medscape and Wolters Kluwer. He reports research support from the American Migraine Foundation, Department of Defense, Henry Jackson Foundation, National Institutes of Health, Patient Centered Outcomes Research Institute (PCORI) and Sperling Foundation. He reports leadership or a fiduciary role in other boards, societies, committees or advocacy groups (paid or unpaid) for the American Brain Foundation, American Migraine Foundation and International Headache Society Global Patient Advocacy Coalition. He reports stock options/shareholder/patents/board of directors for AYYA Biosciences (options), Atria Health (options), Aural Analytics (options), Epien (options/board), ExSano (options), Healint (options), King-Devick Technologies (options/board), Man and Science (options), Matterhorn (shares/board), Nocira (options), Ontologics (shares/board), Precon Health (options/ board), Second Opinion/Mobile Health (options), Theranica (options). He reports patent 17189376.1-1466:vTitle: Botulinum Toxin Dosage Regimen for Chronic Migraine Prophylaxis (non-royalty bearing); patent application submitted: Synaquell (Precon Health). RCC reported royalties from Houghton Mifflin Harcourt; compensation for expert legal opinion to the National Collegiate Athletic Association and National Hockey League; consults for the Concussion Legacy Foundation; is senior advisor and paid consultant to the NFL Head Neck & Spine Committee; is a member of the Mackey-White Committee of the National Football League Players Association; is vice president of National Operating Committee on Standards for Athletic Equipment and chair scientific advisory committee and cofounder of Medical Director Concussion Legacy Foundation; and is on the Medical Science Committee for the National Collegiate Athletic Association Student-Athlete Concussion Injury Litigation. DHD serves as an expert witness in legal cases involving brain injury and concussion and serves as an advisor and options holder for StataDx outside the submitted work.

  • Provenance and peer review Not commissioned; externally peer reviewed.