Pediatric Traumatic Brain Injury: Past, Present and Future

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1 Pediatric Traumatic Brain Injury: Past, Present and Future Christopher King, MD, FACEP Professor of Emergency Medicine and Pediatrics Albany Medical College Definitions Severe TBI causes significant structural brain abnormalities and results in permanent dysfunction or death. Minor or mild TBI has a multitude of definitions and terms, which has led to confusion both in terms of clinical management and research efforts. Probably the best definition of minor TBI is head injury with transient altered MS. Patients with minor TBI are generally expected to have complete recovery within one year. While many definitions of minor TBI have included LOC as one of the requirements, more recent evidence suggests that 80 to 90% of cases do not involve LOC and that LOC does not predict severity of symptoms. Minor TBI is often called concussion in the lay press and sports literature (also ding, bell ringer ), but one study showed that when this term is used, families may not understand that injury to the brain has occurred, possibly leading to premature return to normal activity and sports. Immediate Injury Characteristics of Minor TBI Loss of Consciousness (and duration) Amnesia Amnesia Before (Retrograde) Are there any events just BEFORE the injury that the injured person has no memory of (even brief)? Amnesia After (Anterograde) Are there any events just AFTER the injury that the injured person has no memory of (even brief)? Other Observed Immediate or Early Mental Status Changes or Neurologic Features Altered mental state, confusion or disorientation o Appears dazed or stunned o Answers questions slowly o Is confused about events o Repeats Questions o Forgetful (recent information) Seizures

2 Algorithm for Diagnosing Minor TBI Categories of Typical Minor TBI Symptoms PHYSICAL Headache Nausea/Vomiting Balance Problems Dizzinesss Blurred Vision Fatigue Sensitivity to light or noise Numbness/Tingling Dazed or Stunned EMOTIONAL/BEHAVIORAL Irritability Sadness More emotional Nervousness COGNITIVE Feeling mentally foggy Feeling slowed down Difficulty concentrating Difficulty remembering Forgetful of recent information or conversations Confused about recent events Answering questions slowly Repeating questions SLEEP Drowsiness Sleeping more than usual Sleeping less than usual Trouble falling asleep

3 Epidemiology TBI is the leading cause of death and disability in childhood in developed countries, resulting in 2500 pediatric deaths and 17,000 cases of permanent neurologic dysfunction annually in the US. Poor neurologic outcome often results in many years of care requirements for these patients, and because so many young people are affected, the number of productive person years lost to society is enormous. The total annual cost estimate in the US is $12 to $15 billion. The population effects of minor TBI are more difficult to quantify. It is estimated that there are at least 200 cases annually per 100,000 children (> 150K), although many cases are unreported. It is believed that the effects of multiple injuries are in some way additive in terms of injury to the brain. However, the extent and prevalence of morbidity associated with minor TBI are unknown. Basic Principles Primary brain injury occurs at the time of the initial traumatic event and can only be affected by prevention. Secondary brain injury occurs any time after the event and includes both injury progression and iatrogenic factors (things we do or fail to do). Cerebral perfusion pressure (CPP) is dependent on mean arterial pressure (MAP) and intracranial pressure (ICP) as follows: CPP = MAP ICP. Cerebral autoregulation maintains an appropriate cerebral blood flow over relatively wide ranges of blood pressure and ICP but fails when the BP is too low/high or the ICP is too high. Injury Mechanisms The two ways that force is imparted to the brain are acceleration deceleration and rotational. Both of these types of forces may occur during a traumatic event. Acceleration deceleration cause the rigid skull to stop or accelerate quickly while the brain continues to have relative movement. This causes a skull brain collision with brain deformation and resulting injury. Rotational injuries result when a pivot point occurs causing the head to spin forcefully along an axis. This movement produces shear forces that cause injury when deeper structures in the brain move relative to more superficial structures. Rotational injuries often affect the axons and in extreme cases produce diffuse axonal injury. The resulting injuries that occur include cerebral contusions of varying severity, subarachnoid hemorrhages, subdural hematomas, epidural hematomas as well as diffuse axonal injury. Mechanisms of Brain Cell Death Caused by Severe TBI Brain cells die after TBI by multiple mechanisms/pathways. Cytotoxicity refers to the direct effects of free radicals, exitatory amino acids, etc. released after injury. Apoptosis refers to programmed cell death in which an undetermined switch is thrown that destines a cell to die despite any changes for the better. Much research has focused on delineating the mechanism of apoptosis. Ischemia due to impaired O 2 utilization or delivery may also result in cell death after TBI. Pathophysiology of Minor TBI Animal studies suggest that minor TBI results in a complex cascade of neurometabolic changes ( energy crisis ). Factors include a release of neurotransmitters, unchecked ion shifts and altered glucose metabolism. In humans, advanced imaging modalities (MRS, SPECT, PET) have demonstrated perfusion and metabolic abnormalities as well as axonal injury.

4 Unique Aspects of Severe Pediatric TBI While brain injuries in children are similar to those in adults, there are some important differences. For one, children are much more prone to severe, diffuse cerebral edema after TBI than are adults. In addition, the concept of plasticity plays a role in the developing brain. For many conditions involving the brain, plasticity results in a rewiring of functions that have been lost so that another area of the brain develops the capability of performing the lost functions. In other words, the brain of a child is not as hardwired as that of an adult. This would be expected to result in more favorable outcomes in children after severe TBI. However, the youngest children (< 4 years), who have the greatest degree of plasticity, uniformly do worse than older children with the same type of injury. Another unique aspect of pediatric TBI is abusive injuries which, unlike other types of TBI, have many of the characteristics of ischemic brain injury. One of the most challenging aspects of abusive injury is that the mechanism described to health care providers is often intentionally misleading. Preventing Secondary Brain Injury After Severe TBI From a clinical standpoint, our most important goal is to prevent secondary brain injury. The most effective ways of doing this are: (1) maintain adequate oxygen delivery (BVM, intubation); (2) maintain adequate blood pressure (fluids, blood, pressors); (3) prevent intracranial HTN leading to herniation (if necessary, with hyperventilation, as with an expanding epidural hematoma); (4) avoid inappropriate hyperventilation, which in extreme cases may cause excessive vasoconstriction and ischemia; and (5) avoid hyperthermia (fever). While fever is not usually a problem with TBI patients in the ED (more common in the ICU), good evidence suggests that fever worsens brain injury and should be treated with antipyretics if it occurs. Clinical Care While our ability to provide supportive critical care to TBI patients has advanced dramatically, we still have no specific therapies for TBI. This deficiency in our clinical armamentarium persists despite recent breakthroughs for other types of brain injury (post cardiac arrest, stroke). So our current dilemma is that TBI is a major public health problem for which we have no treatments. Several factors have played a role in this. Significant challenges exist for both laboratory and clinical research with regard to TBI in children that have resulted in a failure to translate effective therapies from bench to bedside. Challenges for Laboratory Research Much of the laboratory research that has been done on TBI has focused on finding a mechanistic magic bullet, i.e., a pathway that, if blocked, will prevent injury. However, the complexity of the brain makes it unlikely that such an individual pathway exists. Additionally, for reasons of expense and logistics, the vast majority of laboratory studies on TBI have used rodents, despite the fact that the brain of a rodent differs from that of a human in several important ways, e.g., small cerebral cortex, minimal white matter tracts, lissencephalic (no gyri and sulci). Furthermore, cognitive outcome measures for rodents may not adequately reflect executive function tasks that are important in human outcomes after brain injury, and the injury mechanisms used in the laboratory, while reproducible, do not represent the types of injuries seen in most human patients.

5 Challenges for Clinical Trials With severe TBI, there are often other significant injuries which serve as confounders. When a patient has multisystem trauma and hypotension, it makes determining the effect of a therapy on protecting the brain far more difficult. There is also wide variability in the brain injuries that people sustain (any combination of contusion, hematoma, axonal injury, etc.) making for a heterogeneous patient population. Furthermore, there is currently no robust injury classification system for TBI, and as such, it is difficult to compare apples to apples in study subjects. We need a system of classification in TBI similar to the staging of cancers that is used for cancer research. Clinical trials for minor TBI have the challenges of determining exactly how severe the concussion was, since we have no readily available tests to tell us and must rely on acute symptoms and descriptions of the mechanism. Outcomes after minor TBI are also largely subjective, and currently available neurocognitive testing is an imperfect tool. Clinical trials for pediatric patients in general suffer from the public s desire to protect children from experimentation. This attitude has contributed to the fact that there are relatively few randomized trials in children, which has resulted in them truly being therapeutic orphans, with much of the treatment for children based on extrapolations of data from adults. Pediatric TBI clinical trials are also hampered by barriers to enrollment and initiation of experimental treatment soon after injury (when a therapy is most likely to have an effect) such as the time required for stabilization and diagnosis in children with multisystem trauma and the common need to transport a child to a tertiary center. Biomarkers These are proteins which are released after injury that cross the blood brain barrier and enter the peripheral circulation. Examples include S100B, myelin basic protein, neuron specific enolase, cleavedtau protein, etc. Biomarkers could be extremely useful clinically for applications such as predicting outcomes (distinguishing a bad concussion from no brain injury at all) and determining who does and does not require a head CT scan. Unfortunately, the biomarkers that have been studied in children thus far have not shown adequate sensitivity and specificity for such uses. Hypothermia for TBI Hypothermia has been used sporadically as a therapy for TBI for decades. It has come in and out of favor multiple times over the years. We have learned that deep hypothermia (< 30 C) causes too many complications, and for this reason, recent studies have focused on using mild or moderate hypothermia. Many have believed that hypothermia is the most promising potential therapy for TBI, in part because animal studies have universally shown a benefit. Furthermore, recent evidence has shown that hypothermia is effective in treating brain ischemia after cardiac arrest and in neonates with hypoxicischemic encephalopathy. However, the results from clinical trials have been mixed at best. In 2005, Adelson, et al. conducted a phase II trial that consisted of the following: (1) Age < 13 years (n = 48); GCS 8; enrollment < 6 hours post injury; moderate hypothermia (32 C to 33 C) for 48 hours. They found decreased mortality in the hypothermia group (17% vs. 5%) for patients < 16 yrs who had cooling initiated within 6 hrs (excluding the most severe group), decreased ICP in the hypothermia group during the first 72 hours (although rebound elevation after rewarming), and a trend toward improved neurologic function during 3 to 6 month follow up. There were increased arrhythmias in the

6 hypothermia group, but they were mild and stopped with rewarming. There were no differences between the groups in terms of other complications. This was the first randomized control trial evaluating hypothermia as a treatment for pediatric TBI, the results of which appeared promising. However, Hutchison, et al. published a study in the NEJM in 2008 that not only showed no benefit, but potential harm. The study used the following methods: age 1 to 17 years (n = 225); GCS 8; moderate hypothermia (32.5 C) for 24 hours; enrollment < 8 hours post injury; outcome assessed at 6 months. The found that there were more unfavorable outcomes (severe disability, persistent vegetative state, death) in the hypothermia group (31% vs. 22%, P=0.14). There were more deaths in the hypothermia group (21% vs. 12%, P=0.06). There was also more hypotension (P=0.047) and more use of vasoactive agents (P<0.001) in the hypothermia group. The Hutchison study received a fair amount of criticism. The fact that cooling was only done for 24 hours and that rewarming was completed in less than 24 hours was thought to be too short of a time interval. The initiation of cooling was also highly variable, from 1.6 to 19.7 hours after injury. There was more hypotension and hypoxia on study entry in the hypothermia group, indicating a problem with randomization that led to the hypothermia group being sicker prior to treatment. There were also questions about the management of the two groups the normothermia group received more mannitol and hypertonic saline (suggesting more aggressive treatment of elevated ICP) and the hypothermia group had persistently low BP and cerebral perfusion pressure for up to 72 hours (indicating inadequate treatment). The Cool Kids trial was designed to avoid these criticisms. It consisted of: age < 16 years; GCS 4 8 post resuscitation; cooling initiated within 6 hrs of injury; hypothermia for 48 hours with slow rewarming. The primary outcome was mortality at 3 months. The study was planned for enrollment of 360 patients. However, it was recently stopped due to lack effect on the primary outcome. Whether further trials will be conducted to assess the effect of hypothermia as a treatment for severe pediatric TBI is now questionable. Future Directions Areas for future study include (1) better laboratory models; (2) improved injury classification; (3) more sensitive and specific biomarkers; (4) early advanced imaging for minor TBI; (5) genomics/proteomics; (6) new drugs (citicoline, progesterone, amantadine) and drug cocktails; and (7) novel therapies (e.g., stem cells). References Adelson, P.D., Ragheb, J., Muizelaar, J.P., Johnson, D., Kanev, P., Brockmeyer, D., Beers, S., Brown, S.B., Cassidy, L., Chang, Y., and Levin, H. (2005). Phase II clinical trial of moderate hypothermia following severe traumatic brain injury. Neurosurgery 56, Hutchison, J., Ward, R., Lacroix, J., He bert, P., Skippen, P., Barnes, M., Meyer, P., Morris, K., Kirpalani, H., Singh, R., Dirks, P., Bohn, D., Moher, D., HyP HIT Investigators, and Canadian Critical Care Trials Group. (2008). Hypothermia therapy after traumatic brain injury in children. N Engl J Med 358,

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