Herniation syndromes

One of the most important, time-critical, and potentially fatal complications of brain injury with increased intracranial pressure (ICP) is brain herniation, which, if untreated in a timely manner, can quickly lead to irreversible brain injury and death. Brain herniation is defined as the displacement of brain matter from its normal anatomical compartment into a different one and sequential compression of adjacent structures. The underlying mechanism of this phenomenon can be explained by the Monro-Kellie doctrine, which states that the sum of volumes of brain parenchyma, blood, and cerebrospinal fluid (CSF) is constant, and an increase in one of these components should be counterbalanced by a decrease in one or both of the remaining volumes. Brain herniation in TBI occurs when there is an occupying lesion (e.g., intracranial hematoma) causing an increase in ICP, presence of cerebral edema, and subsequent displacement and compression of the brain parenchyma.

Herniation syndromes are classified based on their location as either supratentorial or infratentorial ( Figs. 12.1 and 12.2 ).

(A) Schematic representation depicting normal cerebral structures in a coronal plane. (B) Left-sided uncal herniation resultant from epidural hematoma. (C) Central herniation represented by downward displacement of the diencephalon. (D) Subfalcine herniation represented by cingulate gyrus displacement under the falx cerebri and associated transcalvarial herniation through a skull defect.

(A) Coronal computed tomography (CT) image of a normal brain. (B) Coronal CT image of a patient who suffered from extensive intracranial bleed and cerebral edema requiring decompressive craniectomy with resultant subfalcine, uncal, and transcalvarial herniations.

Supratentorial herniation syndromes include uncal, subfalcine, central transtentorial, and transcalvarial herniation. Infratentorial herniation syndromes include tonsillar and reverse transtentorial herniation.

This chapter will discuss the four main types of herniation associated with TBI: uncal, central transtentorial, subfalcine, and tonsillar herniation.

Uncal herniation

Uncal herniation is the most common type of cerebral herniation and develops when the medial portion of the temporal lobe (uncus) protrudes downward through the tentorial notch, compressing the midbrain ^{, ,} ( Figs. 12.1 and 12.3 ). At early stages the clinical presentation is mainly ophthalmic, with paralysis of the third cranial nerve (oculomotor nerve) first causing an ipsilateral fixed and dilated pupil that will later progress to complete ptosis and a characteristic “down and out” gaze. As herniation continues, the ipsilateral superior cerebral peduncle and posterior cerebral artery become affected, leading to contralateral hemiparesis followed by decerebrate posturing and visual cortex infarction with subsequent cortical blindness. ^, The ascending reticular activating system (ARAS) can also be compromised, and alteration of consciousness will ensue. ^,

Coronal computed tomography image demonstrating left-to-right uncal displacement (red arrow).

Subfalcine herniation

The cingulate gyrus can herniate under the free edge of the falx cerebri when an occupying lesion in one of the cerebral hemispheres begins expanding, giving rise to what is known as subfalcine herniation ( Figs. 12.1 and 12.4 ). Ropper et al. have established a direct correlation between the degree of horizontal shift of the pineal gland and the level of consciousness. When there is a pineal gland shift of 6 to 9 cm, stupor appears, and when the shift is greater than 9 mm, it is associated with coma. Progression of the herniation may result in compression of the pericallosal and callosal marginal arteries, medial temporal lobe infarction, and obstructive hydrocephalus caused by compression of the foramen of Monro.

(A) Coronal and (B) axial computed tomography image of a patient with a large subdural hematoma with associated subfalcine herniation (red arrows).

Tonsillar herniation

Tonsillar herniation occurs when the cerebellar tonsils protrude downward through the foramen magnum and can lead to coma, flaccid paralysis, and cardiorespiratory failure caused by compression of the lower medulla ^, ( Fig. 12.5 ). This type of herniation carries a high mortality rate. ^, The mainstay of treatment for herniation syndromes post-TBI is immediate surgical decompression. If clinical signs are rapidly recognized, the chances of a favorable outcome with the appropriate treatment are significantly improved. Herniation secondary to head injury tends to have the worst outcome, and the prognosis depends not solely on the timing of surgery but also on other intracranial and extracranial injuries.

Sagittal computed tomography image of a patient with cerebellar tonsillar herniation (red circle).

Second-impact syndrome

Second-impact syndrome (SIS) is defined as a specific form of cerebral swelling resulting from a second brain injury (usually mild) occurring before symptoms associated with the initial insult have fully resolved. The classic scenario is an athlete who sustains a concussion, returns to play before postconcussion symptoms have resolved, sustains a second hit (whether a concussion or a simple tackle that applies acceleration–deceleration forces to the brain), and within 2 to 5 minutes drops to the ground, develops respiratory failure, brain herniation, and catastrophic brainstem compression. Possibly one of the most controversial and poorly understood complications of brain injury, SIS can be fatal, resulting in rapid brain herniation within minutes of the second hit and death, making it of vital importance to understand its underlying mechanisms and possible forms of prevention.

This syndrome, mostly seen in athletes and caused by repeated concussions and early return to play (RTP), is hypothesized to be the result of two different mechanisms:

• 1.
  

  Altered metabolism and neuronal cell damage: After a first hit, cerebral protein synthesis is decreased, free radical formation develops, lactic acid starts to build up in the neuronal cells, and extracellular potassium massively increases, subsequently leading to cerebral edema. ^{, ,} At this point the brain has entered a state of hypermetabolism that can last up to 10 days. ^, These metabolic changes make the brain more susceptible to a fatal outcome as a result of subsequent injuries, regardless of their severity. ^,

  
  
• 2.
  

  Vascular congestion: The brain’s vasculature ability to autoregulate after a first TBI is impaired, leading to increased cerebral blood flow, consecutive vascular engorgement, and resultant edema. When a person receives a second hit before symptoms of the first concussion have completely resolved, the brain is still in a state of autoregulatory impairment, and the existing vascular congestion worsens and is further enhanced by trigeminal system dysfunction. ^{, ,} The reason behind the belief that a trigeminal system failure exacerbates cerebral vascular congestion is that when a head trauma occurs, the trigeminal system becomes stimulated, releasing vasoactive peptides such as substance P, neurokinin A, and calcitonin gene-related peptide, which in turn produce vasodilation and increased vascular permeability. The results of these vascular and neurogenic disturbances are increased ICP, uncal and/or tonsillar herniation, and rapidly ensuing brainstem failure.

An important factor affecting the development of SIS is the time elapsed between the first TBI and the second hit. Some authors argue that the second impact must occur within 10 days of the first one, given that the disruption of neuronal metabolism caused by the first concussion is thought to last this long. Other authors believe that the second hit can happen beyond 10 days after the first concussion and still lead to SIS, which is why RTP is recommended until postconcussion symptoms have fully resolved.

The most effective prevention strategy of SIS is delaying RTP until symptoms of the first concussion have fully resolved, despite the time elapsed from onset. Given the findings in animal studies that vascular congestion as a result of mild TBI (mTBI) is often extremely difficult to control, those who sustain the controversial SIS usually have a catastrophic result.

Postconcussion syndrome

After sustaining a TBI, patients usually report an array of symptoms—some immediate and some late onset—known as postconcussion symptoms . These include somatic, cognitive, and/or emotional symptoms, such as headache, dizziness, nausea, memory impairment, fatigue, sleep disturbances, difficulty concentrating, anxiety, irritability, sensitivity to noise and/or light, depression, and cognitive deficits. ^, These postconcussion symptoms are usually more prominent in the acute and subacute phases of the TBI and fully resolve within a few weeks to 3 months postinjury. When at least three of those symptoms have not resolved by 3 months, are the result of a TBI, create attention or memory deficits on neuropsychological testing, and result in significant social or occupational functioning impairment, they become part of the persistent postconcussion syndrome (PCS) or postconcussion disorder (PCD), according to the Diagnostic and Statistical Manual of Mental Disorders 4th edition (DSM-IV) criteria. ^, Another criterion widely used to diagnose PCS is the one imposed by the International Classification of Diseases 10th edition (ICD-10), which requires the syndrome to follow a TBI with at least three of these symptoms: headache; memory impairment; difficulty concentrating; insomnia; intolerance to stress, emotion, or alcohol; fatigue; dizziness; and irritability. A consensus of which criteria to use has yet to be reached, making incidence of PCS difficult to accurately estimate.

Postconcussion symptoms are divided into four domains: somatic, cognitive, sleep, and emotional.

Posttraumatic epilepsy

Posttraumatic epilepsy (PTE) continues to be one of the most common and disabling complications of TBI, with the particular feature that there is no current effective prophylaxis, and once it develops, seizures tend to be refractory to treatment. Seizures after a TBI are fairly common regardless of the severity and have been classified as immediate (happening <24 hours postinjury), early (happening >24 hours but <1 week postinjury), or late (>1 week after injury). ^, PTE is defined as the occurrence of at least two unprovoked late-onset seizures associated with TBI. Although antiepileptic drugs (AEDs) are routinely administered post-TBI to prevent posttraumatic seizures (PTS) in the immediate and early stages, there are no data that support the use of prophylactic AED to prevent the development of PTE. ^{, ,}

Studies have shown that the severity of the brain injury directly correlates with the risk of developing PTE, with intracranial hematoma, skull fracture, penetrating brain injury, and loss of consciousness or posttraumatic amnesia lasting greater than 24 hours being the major determinants. ^, Age has also been associated with the appearance of late-onset seizures, with younger patients being at higher risk. ^,

The mechanism behind posttraumatic seizures is thought to be a combination of persistent neuroinflammation, which has been linked to the development of PTE, and increased neuronal excitability, believed to be the cause of early onset seizures caused by increased hippocampal glutamate excitotoxicity. ^,

It is of critical importance to continue developing research methods that will better elucidate the epileptogenic process post-TBI. As with many other complications of brain injury, PTE remains poorly understood, with several promising preclinical model studies aiming to develop the preventive therapy that this brain injury complication so desperately needs.

Chronic traumatic encephalopathy

Multiple TBIs have been associated with the development of a neurodegenerative disease called chronic traumatic encephalopathy (CTE). CTE is characterized by an array of symptoms encompassing four domains—cognitive, behavioral, memory, and executive function—and specific neuropathologic findings that include the presence of perivascular hyperphosphorylated tau neurofibrillary tangles in neurons and astrocytes in the cortical sulci (pathognomonic postmortem finding), beta-amyloid plaques, and white matter degeneration. ^,

CTE has been seen in boxers, soccer players, and military personnel who have been exposed to repetitive brain injuries. The age of onset can vary, ranging from 19 to greater than 65 years, and clinical symptoms usually show approximately 15 years after the exposure to repetitive TBI. Symptoms of this TBI complication are extremely similar to those of PCS, making the clinical recognition of CTE even more challenging.

Stern and colleagues have proposed two different clinical presentations of CTE :

• 1.
  

  Younger age onset (mean age of 35 years): Behavioral symptoms appear first, and cognitive deficits have a late presentation.

  
  
• 2.
  

  Older age onset (mean age of 60 years): Cognitive impairment is the first symptom to appear, with behavioral disturbances appearing later in the disease.

This late-phase complication of repetitive TBI, unfortunately, can only be diagnosed by postmortem neuropathology, and there is currently an increased need for the development of a diagnostic tool to aid in its recognition.

Summary

The spectrum of complications of TBI is overwhelmingly broad—ranging from some that are immediate, rapidly fatal, and require an early recognition of clinical signs—to others that can appear late in the course of recovery and disable the patient for the rest of his or her life. There is a need for more research in this subfield of trauma to successfully develop tools that will aid in prevention of such complications and provide the patient with a better opportunity of having a successful recovery.

Review questions

• 1.
  

  A 46-year-old man presents to the emergency department (ED) after aggravated assault, sustaining multiple blows to the head with a baseball bat and positive loss of consciousness (LOC) of approximately 15 minutes. On examination, his right pupil is 6 mm and nonreactive to light, whereas the left is 3 mm and reactive. He appears obtunded and doesn’t follow commands, for which he is intubated emergently for airway protection. On imaging, he is found to have a left frontotemporal–parietal epidural hematoma with midline shift and uncal herniation. Which of these therapies would most likely treat this complication?

  
  
  
  
  • a.
    

    Elevate head of bed 30 degrees

    
    
  • b.
    

    Intravenous mannitol

    
    
  • c.
    

    STAT operating room (OR) decompressive craniectomy

    
    
  • d.
    

    Hyperventilation to 25 to 30 mm Hg

  
  
  
  
• 2.
  

  A 21-year-old unrestrained male driver presents to the ED after a motor vehicle accident in which he was ejected from the car. Computed tomography (CT) scan of the head shows a large right temporal epidural hematoma, and he undergoes an emergent decompressive hemicraniectomy. An external ventriculostomy device is placed for intracranial pressure monitoring, and he is transported to the neurointensive care unit (NeuroICU) for further management. He remained intubated and sedated on propofol. Three hours later, the patient shows a decerebrate posturing, and on examination, his pupils are fixed and dilated. Repeat CT head scan is performed. What will the scan most likely show?

  
  
  
  
  • a.
    

    Subfalcine herniation

    
    
  • b.
    

    Tonsillar herniation

    
    
  • c.
    

    New ischemic areas

    
    
  • d.
    

    Central transtentorial herniation and new multiple hemorrhagic areas

  
  
  
  
• 3.
  

  A 23-year-old college football player sustains a blow to the head during a game and experiences brief LOC of approximately 30 seconds. His coach clears him to go back to the game, and within 3 minutes, the player falls to the ground and becomes unresponsive. On arrival to the ED, the patient is not able to breathe, and pupils are fixed and dilated on examination. He is intubated emergently for airway protection and taken for a CT head scan STAT. The scan shows a large frontotemporal hyperdensity and central transtentorial herniation. Within minutes, the patient as a cardiac arrest, resuscitation efforts are unsuccessful, and he subsequently dies. What relevant medical history will this patient most likely have?

  
  
  
  
  • a.
    

    Previous recent concussion with persistent postconcussive symptoms

    
    
  • b.
    

    Polycystic kidney disease with multiple Berry aneurysms

    
    
  • c.
    

    Transient ischemic attack

    
    
  • d.
    

    Meningioma

  
  

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• 4.
  

  A 34-year-old woman without relevant medical history is involved in a motor vehicle collision in which she was an unrestrained driver and susains a blow to the head with posttraumatic amnesia (PTA) and LOC of approximately 5 minutes. On arrival to the ED, a head CT shows bilateral frontal contusions and a small left subdural hematoma. She is started on prophylactic phenytoin and admitted to the NeuroICU for observation. Her hospital course of stay is uneventful, and she is discharged home in a stable condition 48 hours later. Two months later, the patient presents to clinic with complaints of three occurrences of generalized tonic–clonic seizures that started a month after her TBI. Why did this patient sustain three tonic–clonic seizures despite prophylactic phenytoin?

  
  
  
  
  • a.
    

    The patient had undiagnosed underlying epilepsy.

    
    
  • b.
    

    Prophylactic antiepileptic drugs (AEDs) post-TBI have not been shown to prevent the development of posttraumatic epilepsy.

    
    
  • c.
    

    The patient wasn’t compliant with her treatment post-TBI.

    
    
  • d.
    

    Prophylactic intravenous fosphenytoin wasn’t started promptly on her arrival to ED.

  
  
  
  
• 5.
  

  An 18-year-old boxer sustains multiple blows to the head during a boxing match followed by alteration of consciousness and subsequent LOC for approximately 30 seconds. The on-call sports medicine physician diagnoses him with a mild TBI (mTBI) and advises him to delay RTP until his postconcussive symptoms fully resolve. In the following days, the patient complains of mild headaches, sensitivity to light, and occasional dizziness but feels well enough to return to boxing. During a match 5 days postconcussion, the patient sustains three more blows to the head and within 2 minutes falls to the ground unconscious, and cardiopulmonary arrest follows. Resuscitative efforts are unsuccessful, and the young man dies shortly thereafter. What is the mechanism behind this patient’s mTBI complication?

  
  
  
  
  • a.
    

    Multiple new brainstem hemorrhages

    
    
  • b.
    

    Cerebral hyperemia and altered neuronal metabolism

    
    
  • c.
    

    Cerebral vasospasm

    
    
  • d.
    

    Cerebral hypometabolic state