Second Impact Syndrome

Gary Goldberg and William A. Robbins

GENERAL PRINCIPLES

Definition

Second impact syndrome (SIS) is defined as a circumstance in which cerebral hyperemia (CHE) leading to diffuse cerebral swelling (DCS) rapidly develops when a person suffers a second traumatic brain injury (TBI) before symptoms related to an earlier initial TBI have fully resolved [1,2]. The second injury typically occurs within 2 weeks after the first impact, with the response being well out of proportion to the severity of the second trauma, presumably due to the influence of unresolved pathophysiology resulting from the first injury. In the pediatric literature, a very similar phenomenon in which CHE precipitates posttraumatic DCS has been labeled “the syndrome of malignant brain edema (SMBE)” [3], a condition for which a solitary TBI suffices. A typically reversible exaggerated neurological response to head trauma in children, linked to enhanced cortical spreading depression (CSD) and CHE, has been called “juvenile head trauma syndrome (JHTS)” [4]. The likely significant pathophysiologic overlap between these three entities, each associated with excessive vasodilatation (EVD) and CHE—SIS, SMBE, and JHTS—along with data from the limited number of well-documented published cases of SIS, implies that SIS prevention, which, in contact sports drives postconcussion return-to-play guidelines, concussion legislation, and the use of computerized neuropsychological testing programs for postconcussion assessment, has a questionable scientific foundation [5]. Several papers have pointed to the dearth of definitive evidence supporting the existence of SIS [6–8]. On the other hand, the CHE-related neurological impairment associated with SMBE and JHTS is a rare but generally acknowledged clinical phenomenon, occurring primarily in children and young adults, where widespread cortical impairment ensues in the context of persisting EVD, CHE, and increased intracranial blood volume [3,4,9]. To address this controversy without rejecting SIS altogether, it may be best to reconceptualize SIS as a rare but particularly severe and lethal variant of traumatically induced CHE leading to DCS, to which increased vulnerability is conferred by the initial head injury. One may consider JHTS, SMBE, and SIS as entities with a common pathophysiology on a spectrum of increasing irreversibility, respectively. The corresponding poor prognosis in SIS may be linked to persistent “second-impact dysautoregulation” [10], wherein the frequent presence of typically insubstantial thin subdural hemorrhage (SDH) amplifies this pathophysiological process [10–12].

Epidemiology

SIS has most often been reported in witnessed sport-related brain injuries. True SIS is exceedingly rare with estimated incidence of a single case every 205,000 player-seasons [13]. From 1984 to 2011, the U.S. National Center for Catastrophic Sports Injury Research in Chapel Hill, NC, identified 164 cases of significant brain injury with incomplete recovery occurring in high school and college football [14]. The computed incidence rate in 2011 for high school football players with permanent brain damage was 0.86 per 100,000 participants. This survey reported one verified case in 2010 of SIS in a 15-year-old who required surgery to evacuate a SDH after suffering a concussion in a head-to-head tackle while still symptomatic from a witnessed concussion that occurred 3 weeks prior [14]. Another study of American high school and college football players reported 94 catastrophic head injuries over a period of 13 academic years from 1989 to 2002 [15]. These injuries were associated with subdural hematoma in 75 athletes, subdural hematoma with DCS in 10 athletes, DCS alone in 5 athletes, and ruptured arteriovenous malformation or aneurysm in 4 athletes. In 59% of these injuries, the athlete had a history of a previous head injury, of which 71% occurred within the same season as the catastrophic event. Thirty-nine percent of these athletes (21 of 54) were playing with residual neurologic symptoms from the previous head injury. There were 8 (9%) deaths, 46 (51%) permanent neurologic injuries, and 36 (40%) serious injuries with full recovery. Most players sustained the injury from head-to-head contact in tackling.

In the only systematic review of this topic, a total of 17 cases of reported SIS were identified in the world literature [16]. Of these only five cases actually involved a repeated injury, and all of these occurred within 7 days of the initial injury [16]. Sport-related SIS most often occurs in young males engaged in contact sports such as boxing, football, and ice hockey [17].

The scenario in which a young, previously healthy individual suffers rapid and dramatic neurologic deterioration indicates that SIS and other injuries in which DCS develops must still be considered a serious and potentially avoidable consequence of head trauma. While rigorously confirmed cases of SIS may be rare, the general notion that an individual should not be permitted to re-engage in high-risk activity until postconcussion symptoms have completely resolved remains difficult to refute [18].

Pathophysiology

Initial transient response to a significant concussion can involve brief vasodilatation, and increased intracranial blood volume. To counteract the tidal wave of blood being pumped to the head by the stress-induced cardiovascular reaction, an initial autoregulatory acute “Phase-I” cerebrovascular response involves intense vasoconstriction and a resulting reduction in cerebrovascular capacitance with lowered intracranial blood volume. An outright failure or insufficient persistence of this Phase-I reaction, however, leads to EVD, engorgement of the cerebral vasculature, massive CHE, and progressive DCS with vasogenic followed by cytotoxic edema. The resulting elevation of intracranial pressure (ICP) then precipitates rapidly developing inferomedial herniation of the medial temporal lobes and brainstem compression [18,19]. The interval from impact to clinical manifestations of brainstem compression in full-blown SIS can be less than 5 minutes [18]. The intracranial manifestations of DCS, including herniation and potential intracranial hemorrhage, can be demonstrated on CT and MRI when imaging is obtained [20].

Following the Phase-I response, a subacute Phase-II response involves a state of altered cerebral metabolism that may last for several days, involving decreased protein synthesis and reduced oxidative capacity [21]. The heightened vulnerability of the brain during this subacute phase of recovery is associated with a relative inhibition of the acute vasoconstrictive Phase-I response that normally prevents CHE, thus leading to an increased risk of CHE triggered by a second insult. At least two case series [10–12] and a more recent case report of confirmed SIS in a 17-year-old football player with normal noncontrast CT imaging but persisting severe headache after the initial injury [22] have identified SDH as another significant factor contributing to failure of the Phase-I response, resulting in EVD and massive CHE.

Another factor which may contribute to Phase-I failure is migraine-linked posttraumatic vascular instability. Persistent posttraumatic headache may be a particularly important indicator of increased second-impact risk, given that vascular headache and JHTS are both thought to be related to a common pathophysiological mechanism involving anomalous trigeminovascular (TGV) activation [23,24]. The TGV system is directly involved in powerfully biasing toward EVD when the trigeminoparasympathetic (TGPS) reflex is abnormally activated by head trauma stimulating sensory afferents traversing the trigeminal ganglion [24]. This TGV associated EVD has been proposed as the underlying mechanism initiating CHE-related neurological impairment in JHTS [25,26]. Given that sensory collaterals of these same trigeminal ganglion cells innervate vessels in the overlying dura, even a small amount of subdural blood may irritate these autonomic afferents, provoking and potentiating the TGPS reflex response to trauma and amplifying the EVD that initiates this pathophysiological cascade [27]. This, in turn, may explain the frequent incidence of SDH in SIS [10–12,22]. It also suggests that substances which block the TGPS reflex may prevent or slow ominous progression to DCS [27]. While this hypothesis regarding TGPS activation as a putative pathophysiologic mechanism seems plausible, data directly supporting it is limited at this time.

In SIS, progression from EVD to CHE to DCS to herniation can take place across a variable time interval with dramatic neurologic deterioration occurring after an initial brief period of wakefulness following minor head trauma, a clinical scenario that Reilly labelled “Talk and Die” [19,28,29]. With a coincident history of familial hemiplegic migraine, delayed neurologic deterioration unfolds in the presence of a specific form of gene mutation affecting the configuration and function of voltage-sensitive calcium channels in the cerebral cortex [30,31]. While this is a very rare genetic condition, it suggests that vascular headache, JHTS, SMBE, and SIS may share a common pathway toward DCS precipitated by trauma-induced EVD, CHE, and augmented CSD [31]. A recent observational case-control study of 1,342 children presenting with mild head trauma for emergency care found that the proportion of the 33 (2.5%) children diagnosed with JHTS who had first-degree relatives with migraine was significantly greater than that for children without JHTS (odds ratio, 2.69; 95% confidence interval, 1.16–6.22; p = 0.010) [32].

DIAGNOSIS

History

• SIS is established through documentation of two separate sequential head injury events with unresolved symptoms of the first head injury persisting through to the second head injury. Stringent diagnostic criteria for SIS require that the initial head injury be witnessed and medically assessed with confirmed symptomatology persisting through to the second witnessed impact [16].

• SIS is distinguished from repetitive head injury syndrome (RHIS), or chronic traumatic encephalopathy (CTE), in which a person sustains several repeated minor head injuries spread out over time and, as a result, experiences a gradual decline in cognitive, affective, and behavioral function (see Chapter 55).

• SIS is an acute life-threatening neurological emergency seen in young individuals under the age of 18, whereas RHIS/CTE is a chronic degenerative condition typically encountered in adults characterized by the cumulative impairments that gradually accrue over time with repeated concussions [7,33–34].

Clinical Presentation

• In the typical presentation, postconcussion symptoms occur after an initial head injury, but before these symptoms resolve, a second relatively minor blow to the head occurs, frequently without immediate loss of consciousness.

• The individual may appear dazed or confused, but remains awake, verbal, and ambulatory. However, over the next few seconds to minutes, dramatic clinical deterioration ensues.

• There is a precipitous neurological decline with the development of a semicomatose state with rapidly dilating pupils, limited spontaneous eye movement, and respiratory failure.

Physical Examination

• In the unconscious athlete, prompt assessment and stabilization of airway, breathing, and circulation, placement of a cervical collar, and spine precautions are essential.

• Careful neurologic examination is performed including assessment of brainstem function and Glasgow Coma Scale score.

• Examination should focus on identifying evidence of elevated ICP (pupillary response, papilledema, obtundation, etc.).

Neuroimaging Assessment

• Computed tomography (CT) scan: rule out structural damage such as intracranial hemorrhage [35], most typically an acute SDH [10–12,22].

• Magnetic resonance imaging (MRI): offers more structural detail to aid in detecting subtle structural changes associated with raised ICP and herniation but requires significantly more time to complete than CT. More advanced MR-based techniques such as perfusion MRI using arterial spin labeling and diffusion weighted imaging are promising research tools, but not relevant to routine clinical practice at this juncture [36].

• CT angiography and perfusion scanning: while not routinely indicated after MTBI, can detect abnormal cerebral blood flow patterns including posttraumatic CHE as well as any cerebrovascular anomalies (e.g., aneurysm, arteriovenous malformation).

Autopsy Findings

• Diagnosis is definitively made at autopsy: the brain shows diffuse and extensive CHE and DCS, often with evidence of transtentorial herniation.

PROGNOSIS

• SIS is linked to a common pathophysiological process shared with vascular headache, JHTS, SMBE, and “big black brain” syndrome in infants, seen most often in the context of nonaccidental repetitive trauma [37]. In SIS, the susceptibility to trauma-induced EVD is significantly increased by the residual effects of the initial head trauma.

• The prognosis varies with the rapidity and degree to which this process irreversibly progresses from EVD and CHE to DCS, elevated ICP, and herniation. In JHTS, the neurological impairment is typically transient and usually fully reversible within 24 hours, while in SIS it progresses rapidly and irreversibly with devastating consequences, including 50% mortality, with most survivors left with significant permanent neurological disability.

• The presence of subdural blood worsens the prognosis by further amplifying trauma-induced EVD, possibly through stimulation of autonomic sensory afferents from trigeminal ganglion cells innervating dural vessels, producing intensification of the TGPS reflex response [23–27].

TREATMENT

• Treatment must be intensive and cannot be delayed.

• The patient should be immediately stabilized with emphasis on airway management, and neurosurgery consulted.

• Rapidly intubate and institute measures to reduce elevated ICP.

• Treatment of impaired autoregulation of cerebral vasculature in true SIS may be difficult or impossible.

• Emergent decompressive craniectomy and/or craniotomy with evacuation of SDH can be a life-saving measure [10–12,22].

PREVENTION OF SIS IN SPORTS

• The best way to prevent SIS is to reduce the overall incidence of concussion in contact sports through protective equipment, education, and enforcement of rules designed to reduce the likelihood of significant injury (see Chapter 9).

• Any athlete who remains symptomatic following a concussion should not be allowed to return to play. If symptom report is unreliable, or the truthfulness of the patient’s own report of symptoms is in question, remember: “When in doubt, sit them out.”

• Multiple clinical guidelines have been published advising on the timing of return to play and level of participation following a concussion. Such guidelines exist, at least in part, to prevent SIS.

• Physicians with experience in concussion recognition and management should be consulted to evaluate athletes before return to play is authorized, in compliance with concussion legislation in many states.

• There is a tendency for athletes to minimize and under-report persisting postconcussion symptoms, particularly under circumstances where there are significant competitive stakes involved [38]. Education (beginning in the preseason) for the athlete [39] and family members is essential. Education for officials and coaching staff is also very important.

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