David J. Bradbury-Squires
Newfoundland and Labrador, Canada
Concussions are complex, pathophysiological brain injuries that are induced by biomechanical forces1. Concussions affect a substantial portion of the population, as approximately 1.8 – 3.6 million concussions are diagnosed annually in the U.S.A. alone. This appears to be a conservative estimate as many concussions appear to be underreported and/or unrecognized1-9.
Although 85 – 90% of patients with a concussion spontaneously recover within 10 days, a small but clinically significant population will go on to suffer persistent-post-concussion syndrome (P-PCS). P-PCS is characterized by a heterogeneous collection of symptoms (e.g. headache, affective and cognitive disturbances, dizziness, nausea, and fatigue) lasting for at least three months1,10-15. P-PCS sufferers experience considerable decreases in quality of life, as many are forced to retreat from their normal occupational, academic, social, and recreational activities while suffering from an “invisible injury”12,16-18,19.
The diagnosis of P-PCS is challenging due to the subjective, non-specific nature of the symptoms and wide differential diagnosis12,14,20-23 (see Ontario Neurotrauma Foundation guidelines14). Although studies emphasize the importance of both physiological and psychological factors in the pathogenesis of P-PCS13,14,24-27, the majority of the literature on P-PCS in the last 150 years has focused on whether P-PCS is physiological (“organic”) or psychological (“functional”) in origin. This controversy is reflected by the large number of titles proposed to describe the condition (see Evans 199428). The purpose of this review is to describe the conceptualization of P-PCS from Erichsen’s seminal 1866 paper29 onwards, and discuss how the subsequent 150 year historical debate has impacted patient care.
Erichsen first described the modern interpretation of P-PCS in 1866 using the term “railway spine”29, and initiated the debate by stating that “symptoms arising from these accidents have been variously interpreted by surgeons…” (p.49). In 1871, a Prussian compensation law for those injured in railway accidents led to an increase in the number of compensation claims for “railway spine”, many of which were labeled as “compensation neuroses”28. In 1881, Hodges30 used the term “so-called railway spine” due to the subjective and possibly fictitious symptoms. The following year31, Erichsen hypothesized that the symptoms were due to molecular disarrangement, inflammation, or anemia caused by minor injuries to the central nervous system. However, Page’s 1883 book32 disagreed with Erichsen and discussed how these “largely unreal and independent of structural change” (p.235) injuries were the result of malingering. That same year, Putnam33 and Walton34suggested excluding “spinal” from the name, reasoning that an injured cerebrum must be the cause due to the presence of hysteria symptoms33 and attentional problems34.
In 1888, Strumpel described how patients exaggerated their symptoms for compensation28. In 1888-89, Charcot hypothesized that the symptoms were a result of hysteria and neurasthenia, as traumatic emotional shock caused the symptoms to be imprinted in the patient’s mind, leading to the pathological manifestation of symptoms35. Subsequently, Oppenheim rejected the notion of “compensation neurosis”, and introduced the term “traumatic neurosis” to the literature28. In 1892, Friedman suggested that dysfunctional intracranial circulation caused most of the symptoms, suggesting the name “vasomotor symptom complex”28. However, in 1893, Gray elaborated on the ideas of Strumpel36, suggesting that patients exaggerated symptoms to appeal to the medico-legal system.
Although the etiology of P-PCS was never more hotly debated, it appears that little thought was given to how to best treat patients, with palliative care being the most commonly prescribed treatment37. Over the next half century, much of the literature would continue to focus on scientific debate rather than improving patient outcomes.
In 1904, English38 acknowledged that both organic and functional changes could result in P-PCS symptoms, stating “functional changes may be maintained and aggravated by organic lesions” (p.487). However, the complex combined physiological/psychological origin of P-PCS symptoms would not be readily accepted until over 100 years later.
In 1920, Sharpe39 eschewed any physiological contribution to P-PCS, stating that “post-traumatic neurosis” is “solely a functional impairment and in no way associated with an organic lesion or change in tissue” (p. 400). Sharpe hypothesized that some post-traumatic neurosis patients consciously32 or unconsciously35, 40exaggerated their symptoms for financial gain28,36, or suffered from their neurosis due to inherent personality traits or life stressors.
In his 1932 clinical study of 200 head injury patients, Russell41 found that, out of 86 of his persistent symptom patients, only 14 had pending compensation claims as a result of their injury. Similarly to Friedman28, Russell concluded that dysfunctional intracranial circulation was the cause of symptoms in the majority of patients.
In 1942, Lewis & Symonds18 promoted the dualistic nature of P-PCS championed by English38, reasoning that physiological and psychological attributes of late post-concussional syndrome are so intertwined, that to attempt to separate them would be unnatural. Unfortunately, this theory was cast aside just an English’s was38.
In 1945, Reusch & Bowman42 found that patients with P-PCS without structural damage exhibited similar symptoms as non-injured neurotic patients. They concluded that “in late post-traumatic conditions, the importance of organic damage to the brain has been widely overrated.” (p.161). Although psychotherapy began to be recommended42 by those implicating psychological origin of P-PCS, discussion of treatment beyond the “expectant palliative method” (p.408)39 was limited.
Miller’s 1961 influential work “Accident Neurosis”43 claimed that any traumatic neurosis following injury was more likely due to litigation rather than actual injury, and that the incidence of neurosis was in fact related to social status, the nature of employment, personality disorders, and low intelligence. Although Miller briefly acknowledged the possibility of a physiological basis for P-PCS, he argued that a psychological origin had to account for the symptoms as “the most consistent clinical feature is the subject’s unshakeable conviction of unfitness for work…” (p. 922).
In 1966 Taylor44 demonstrated a decreased rate of cerebral circulation in patients with P-PCS, and published a review the following year45 which disputed the evidence presented by Miller43. Merskey & Woodforde46 showed in 1972 that symptom outcomes in P-PCS patients did not depend on compensation proceedings. McKinlay, Brooks, & Bond47 replicated and expanded on these results in 1983, showing few differences between claimants and non-claimants in psychometric scores, return-to-work time, or reported symptoms.
Lishman’s seminal 1988 work16 hypothesized (similar to Reusch et al.42) that symptoms initially were physiologic in origin, and slowly became psychologically-induced over time. Throughout this time period, it became increasingly evident that physiological factors played at least some role in the pathogenesis of P-PCS18,28. Unfortunately, little research in P-PCS during this time period focused on treatment, as the recommendations for treatment (namely, palliative methods) had remained much the same as in 194542.
The literature on P-PCS has increased exponentially since 1990, with much of the evidence supporting a physiologic etiology of P-PCS. In 1997, Jordan48 reported a positive correlation with the Apolipoprotein (Apo) E4 allele and the pathophysiology of chronic traumatic brain injury. The potential link between this allele and other genetic markers to the incidence of concussion, P-PCS like symptoms, and chronic traumatic encephalopathy has, and will continue, to be the subject of intensive research1. In 2001, Giza & Hovda49 proposed the neurometabolic cascade theory of concussion, which hypothesizes that axonal shearing and stretching of neurons results in an initial hyper metabolic milieu, followed by compensatory metabolic depression. Reviews in 200717 and in 201250 discuss these changes and also propose other contributing pathophysiological mechanisms such as dysfunctional regulation of the autonomic nervous system, cerebrovascular constriction17, and prolonged inflammation50. However, others still support the notion of a psychological etiology for P-PCS. In 2011, Meares et al.23 reported no association between mild traumatic brain injury and P-PCS, suggesting that pre-injury anxiety/ depression or post-traumatic stress are more relevant early markers of P-PCS than the injury itself.
Although the debate continues, evidence currently suggests that P-PCS is likely due to a combination of physiological and psychological factors11,12,14,25,27,51,52. Current understanding of P-PCS etiology is best summarized by Macleod25 in 2010, who stated “there is invariably a psychological component to any physical disease, and the potentially malignant influences of psychosocial factors can compound the organic state” (p. 1035).
Our understanding of P-PCS has progressed significantly since Erichsen first described “railway spine” in 186631. From the psychological neuroses described by Sharpe39 and Miller43, to Lishman’s16 initially physiological then eventually psychological hypothesis, to the neurometabolic cascade described by Giza et al.49, and finally to the now accepted combined psychological/physiological theory11,12,14,25,27,51,52, the etiology of P-PCS has, and likely will continue to evolve. Unfortunately for patients with P-PCS, improving outcomes has historically taken a backseat to this debate, as they have been forced to live with considerable decreases in quality of life12,16-19, few effective treatments, and the stigma of malingering43. However, with the recent media attention surrounding lawsuits against the NFL and NHL by former players53, 54, more research on the development of evidence-based treatment programs is probable. Recently, combined medical, physical, and psychological treatment approaches via multi-disciplinary concussion clinics (see Makdissi et al.12) have become more common55-58. Currently, it appears that the best approach to patients with P-PCS is to treat what is treatable11, emphasize a symptom-based approach52, and refrain from falling victim to paralysis-by-analysis. By no means is this a suggestion that future research on the etiology of P-PCS is inconsequential – consider this an emphasis on how to best help the people suffering from this “invisible injury”19.
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The author would like to acknowledge Dr. Jim Connor for guidance in developing this manuscript, and Mr. Greg Pearcey and Mr. Matt Eagles for proofreading and editing, and Concussion-U for support throughout.
DAVID BRADBURY – SQUIRES is a third year medical student at Memorial University of Newfoundland. Prior to medical school, David obtained a Bachelor of Kinesiology (Honors) and a Master of Science in Kinesiology at Memorial University of Newfoundland. David is also a Certified Exercise Physiologist with the Canadian Society for Exercise Physiology. In 2013, David and four other medical students founded Concussion-U, which is a concussion education and community engagement group in Newfoundland and Labrador that aims to educate youth athletes about concussion in sport across Atlantic Canada.