Repetitive mild traumatic brain injuries in children of abuse

Abstract

Children experiencing violence is an unsettling reality occurring regardless of sex, gender, age, or socioeconomic status.1, 2 Each of our communities has friends, neighbors, and coworkers who are overlooked daily despite established factors helping to predict those at risk for experiencing abuse.3 Children present in homes experiencing domestic violence are at increased risk of being harmed, with one in three children being abused.4 Physical injuries may be the result of being a primary target, an unintentional bystander, or a human shield.5 When forces are directed to the head and neck, abusive head trauma (AHT) and traumatic brain injury (TBI) occur, resulting in chronic, life-altering injuries. The incidence of AHT is challenging to quantify but is suspected to occur in at least 1000–1500 infants per year (in the United States), with a peak incidence in males at 1 year of life (although increased in males ages 0–9 years old).6 In the most severe instances, AHT is a leading cause of morbidity and mortality in children under 5 years of age.7 Yet TBIs exist on a spectrum of severity. While physical injuries such as bruises and broken limbs are often obvious and dichotomous, repetitive mild traumatic brain injuries (mTBIs) are invisible to the naked eye and may have a delayed onset of signs or symptoms. Often, debilitating symptoms are only realized if inquired about and without any evidence of external, physical injury. Furthermore, children experiencing abuse are more likely to sustain repetitive brain injuries due to prolonged exposure to the abuser. On average, survivors will experience 2–3 years of abuse before they are able to escape the inciting individual.8 Survivors of child abuse thus experience a combination of repetitive mTBI, delayed diagnosis, and improper rehabilitation that increases their risk for developing debilitating cognitive, behavioral, and affective disorders. These symptoms make it challenging for children to meet developmental milestones and engage properly at home, in school, and throughout society. Identifying patients with repetitive mTBI due to child abuse must be an initial step toward caring for all pediatric brain injuries. Recently, athletics has been among the more prominent activities discussed that place children at risk for encountering an mTBI. As a result, children participating in sports have received safeguards that have improved detection, treatment, and rehabilitation of mTBI (i.e., concussions). However, our focus on mTBI occurring in the athletic community has overlooked those experiencing mTBIs through trauma, assaults, and violence. It is estimated that TBIs in the context of domestic violence are at least 12 times higher than occupational, recreational, and accidental events.9 Thus, children experiencing abuse are equally at risk for repetitive mTBI but do not receive the same provisions for diagnosis or rehabilitation. The American Academy of Pediatrics (AAP) policy acknowledges the importance of identifying TBI in children who experience abuse and AHT.10, 11 Yet many children who experience abuse go undetected each year by the medical community as only 10% of the three million child protective services referrals are made from medical providers.12 Furthermore, one study suggests that 31% of children were seen by a medical provider after experiencing AHT but had not been diagnosed, taking an average of seven days but ranging up to 189 days and two to nine physician visits to be detected.13 As a pediatric medical community, we must use each encounter with a child to evaluate for suspected abuse. Notrica et al. identify how an unknown number of adults in the home, substance abuse, intimate partner violence (IPV), and prior police involvement each increase the risk for AHT in children under 5 years of age.14, 15 Asking about each of these factors on intake forms or during encounters is a simple way to improve our understanding of those children at risk for abuse. Furthermore, increased collaboration with our dental colleagues will help increase our detection of child abuse as well as improve children's health. The AAP currently recommends that every child visits a dentist at least every six months.16 Dentists are thus uniquely primed to detect signs and symptoms of abuse through intraoral radiographs, perioral trauma (frenulum tears, bone or tooth fractures), facial asymmetry, or manifestations of infection (HIV, gonorrhea, and syphilis).17 Additional safeguards should be established to evaluate a child for abuse and brain injury when a parent is identified to have experienced IPV due to the increased prevalence in this population. While this represents just a few ways to improve our detection, each of these mechanisms can help provide a better understanding of children at risk for abuse and repetitive mild traumatic brain injuries. When assessing the acute presentation of injured children, clinical evaluations must consider brain injuries as a primary or comorbid condition. Data suggest that as many as 61% of individuals who have experienced violence sought care at a health care facility for reasons unrelated to a brain injury but were subsequently diagnosed with a TBI as their primary condition.18 In children (ages 0–18 years), presenting symptoms in those with AHT included fever, dizziness, difficulty breathing, nausea, vomiting, poor eating, extremity concerns (bruises, swelling, and fractures), seizures, and skin concerns.14, 15 These data indicate that even when other external signs are present, AHT and TBI may go undetected. In the context of mTBI, when there are rarely additional external signs of injury, it is thus reasonable to conclude that these children experience at least similar, if not higher, rates of delayed recognition. Additionally, while we often use our own clinical gestalt to determine if further evaluation is needed for abuse or brain injury, these studies suggest that we are poor predictors of this. Each of the above presenting concerns has a broad differential that deserves a medical workup. However, we must remember Hickam's dictum in the setting of suspected abuse. The most common diagnosis given to missed cases of AHT has been viral gastroenteritis, and while some of these were correct, one diagnosis does not preclude abuse.13 Abuse must always be thoroughly considered when evaluating patients with medically unexplained signs and symptoms so as not to miss an opportunity to intervene. When abuse is suspected, we must continue past the visually obvious signs and conduct systematic, consistent, and frequent evaluations of brain injury. Suspicion of AHT or mTBI, particularly in young patients (ages 0–5 years), typically involves head imaging to evaluate for cranial fractures or intracranial bleeds. In these cases, 21% of the scans will result in a normal CT.15 While reassuring for acute processes, these results should not suspend clinical investigation as mTBIs will also have unremarkable head imaging. On the other hand, when acute neurological processes (e.g., hematomas, hemorrhage, infarctions, cranial fractures) are found on imaging, these too should not conclude the workup, as an mTBI is also likely to have occurred. Complicating the AHT diagnosis is that, while evidence of subdural hematomas (SDHs) primarily raises suspicion for abuse, alternative etiologies such as benign enlargement of the subarachnoid space (BESS), stretching/injury of the bridging veins, and cortical vein thrombosis must also be considered.19-22 This is highlighted by an analysis of Norwegian infants suspected to have SDHs via AHT that identified 81% of subdural fluid as chronic based on radiological analysis.23 Additional characterization of this population identified that all (100%) infants who were considered to have BESS additionally had chronic SDHs and were associated with a male predominance and without acute clinical symptoms.23 Ultimately, age-appropriate neurological evaluation is needed in every child with suspected abuse and mTBI regardless of the imaging findings, as mTBI remains a clinical diagnosis. In the past decade, the development of neurocognitive assessments that are administered in the acute period following a suspected brain injury has helped aid the clinical diagnostic process (i.e., Graded Symptom Checklist [GCS], Acute Concussion Evaluation [ACE], Rivermaid Post-Concussion Symptom Questionnaire [RPSQ], Health and Behavioral Inventory [HBI], Post-Concussion Scale [PCS], Immediate Post-Concussion Assessment and Cognitive Testing [ImPACT], and Post-Concussion Symptom Inventory [PCSI]). The nature of repetitive mTBIs secondary to abuse and delayed presentation makes it nearly impossible to know when the most recent brain injury occurred without a direct witness. Therefore, implementing neurocognitive assessments commonly used in the athletic community must be considered with caution. Currently, there is no gold-standard biological or radiographic biomarker to aid in the diagnostic evaluation of mTBI. If a reliable biomarker of brain injury becomes available, this population may benefit from objective diagnostic criteria for treatment as well as medical–legal indications due to the heterogeneous nature of brain injury. At this time, health care providers must consider TBI when evaluating for acute (days to weeks) and chronic (months to years) sequelae in any child suspected of abuse. Brain injury results in a chronic disease process that produces a diverse group of signs and symptoms over time. Difficulties in diagnosing acute mTBIs in children of abuse require clinicians to follow the progression of signs and symptoms to help guide recovery. Acute presentation of mild to moderate brain injury in children ages 2–12 years in the emergency department has indicated that headaches, drowsiness, nausea/vomiting, dizziness/balance problems, confusion, and cognitive symptoms were among the most common initial symptoms in the first 72 hours.24 In the days to weeks after a singular brain injury, individuals ages 12–22 years developed sleep disturbances, frustration, irritability, and forgetfulness after the initial presentation.25 One study found that these symptoms may last up to at least two years following the initial injury, with additional concern for the development of outward behavior problems (hyperactivity, aggression, and conduct problems).26 Furthermore, up to 80% of children who experience TBI via AHT will develop cognitive, behavioral, and affective symptoms.15 These children will need to be monitored for years after the inciting events as disruptions to physiological processes (i.e., endocrinopathies) may present as abnormalities in their development or age-appropriate neurological milestones.27 These studies highlight the chronic nature of brain injury and the need to always inquire about previous episodes of known or suspected brain injury when evaluating for physiological, cognitive, behavioral, or affective concerns in all children. Determining which children will have persistent symptoms after a singular brain injury (much less repetitive mTBI) is difficult. Symptoms may resolve in most children with a single mTBI after a few months, but for those who do not fully recover, the impairment that their symptoms cause in their daily lives makes it extremely difficult for them to participate in school and society. In the context of child abuse, the true impact of each child's repetitive mTBIs is unique and currently unable to be fully quantified. The consequences of repetitive brain injuries, especially those without proper recovery, are concerning for a child's development and long-term health. In the most severe instances, children who experienced AHT were more likely to have a moderate or severe impairment, including learning difficulties, vision problems, and hearing difficulties, as well as cognitive and physical impairments.10, 18, 28 Analogous groups in the adult literature with repetitive brain injuries (such as athletes and military personnel) provide insight into the impact of experiencing repetitive brain injuries without proper recovery. These individuals experienced worse neurological sequelae, including cognitive, behavioral, and affective disorders.29-31 Future studies are needed to determine the impact of repetitive mTBIs in the context of child abuse, as children in these homes are commonly reported to develop a mix of neurological and psychiatric conditions, including cognitive difficulties (i.e., attention-deficit/hyperactivity disorder, difficulty thinking), behavioral difficulties (sleep disturbances, nightmares), and affective disorders (anxiety, depression, posttraumatic stress disorder). Considerable overlap between TBI-induced symptoms and psychiatric disorders as a result of the experienced trauma most certainly exists. Behavioral symptoms such as difficulty coping, delayed milestones, acting out, lack of impulse control, and somatic and psychiatric concerns have all been reported in children who have witnessed domestic violence.32 Previously, these symptoms were commonly thought to be the sole result of the experienced trauma. However, considering the multiple brain injuries these children may have experienced, it is likely that their symptoms are in part due to the chronic pathophysiological process and injury cascades resulting from TBI. As such, this distinction between trauma and mTBI may not be fully elucidated, especially as similar changes to neuronal circuitry have been described between TBI and posttraumatic stress disorder.33, 34 Therefore, a child's behavioral outbursts may be a result of decreased inhibition; their sensitivity to touch, light, or sound; a product of allodynia, photophobia, or phonophobia; and psychiatric challenges as consequences of altered neurocircuitry in the limbic system. Further complicating these children's outcomes is that exposure to an unstable social situation following their brain injury makes it more likely for these children to develop persistent postconcussion symptoms.35, 36 Children who survive child abuse are significantly at risk for social and legal challenges in finding a caregiver (i.e., a nonabusive parent who is able to adequately care for the child after escaping the violent partner or a willing family member), being placed under foster care, and possible involvement in legal proceedings. Overall, this mix of trauma, repetitive mTBI, and challenges after escaping abuse puts these children inherently at an increased risk for developing persistent symptoms after mTBI. As these children become better identified, it is of the utmost importance that we consider the physical (i.e., TBI) and psychological trauma that they have experienced in order to properly treat their symptoms and improve their prognosis and quality of life. Children who have experienced abuse and received repetitive mTBIs benefit from multidisciplinary care. Currently, children who experience observed mTBI are offered a plethora of clinical resources. Often, they are brought to a medical provider (emergency department, urgent care, or pediatrician's office) acutely following the injury and undergo individualized planning to help recover from their brain injury. Neurologists have also created specialized clinics for patients with acute and complex brain injury. Yet the most common patient population referred to these clinics are children who have experienced brain injuries through athletics, observed violence (i.e., fights), or motor vehicle accidents. While other brain injury clinics of other specialties also exist, these clinics often are limited to mTBIs occurring from athletic events and exclude those from motor vehicle collisions, trauma, or abuse. Thus, children who have experienced mTBI as a result of abuse are overlooked and do not receive the care they need. And while we acknowledge that all mild to moderate brain injuries are underreported across the spectrum of TBI, children of abuse have likely experienced more repetitive and undiagnosed brain injuries. As these children recover, they are more likely to have symptoms that may be attributed to their brain injury. Thus, we recommend that these children need and deserve multidisciplinary care. Moving forward, we must begin to treat children of abuse as brain injury survivors. Across the nation, the standard of care for patients with brain injury has begun to be set, with children of abuse often not receiving these essential services. Unfortunately, multiple barriers and health care disparities prevent these children from accessing care. Except in rare instances, children depend on adults for many of their needs, including health care. Barriers such as adult mistrust of the health care system, concerns of losing guardianship of their children, and focus on safety over health care lead too often to children in abusive situations not making it to a health care provider. Further, when resources are able to be obtained, health care for TBI is an institution-specific, resource-dependent, and multidisciplinary effort. Thus, the following outlines our recommendations to improve our care of child abuse and brain injury survivors. First and foremost, children who experience abuse should have a medical home with a trauma-informed pediatrician who can access a child abuse pediatrician for guidance and advice. Second, and in accordance with the AAP's recommendations, specialty-specific care should be consulted where appropriate. When available, this should include neurology, neuropsychology, and developmental–behavioral pediatricians to provide both an initial evaluation and treatment of brain injury as well as scheduled follow-ups for the evaluation of physical development, cognitive development, learning differences, and mental health. We recognize that the prevalence of child abuse does not limit itself to large urban centers with large academic centers for children. In these cases, these patients should be treated alongside the current recommendations for brain-injured children with close monitoring for persistent symptoms. If the child continues to have cognitive, behavioral, and affective symptoms, referral to neurology for complex brain injury would thus be indicated. By enrolling these patients in treatment, a combination of pharmacological and nonpharmacological management can help patients cope with the various symptoms they may experience.37 By doing so, these children will be better able to reintegrate into school, society, and home, but also help prevent future violence when they grow up.38 All brain injuries, regardless of severity, can significantly influence the trajectory of an individual's life. Therefore, every child with a brain injury deserves individualized treatment when recovering. The “return to learn” and “return to life” campaigns that have been primarily considered in the realm of athletic brain injuries must extend to all children who have experienced an mTBI. A multidisciplinary approach must be taken with children who experience physical abuse and TBIs. Initially, this entails improving our detection of children who have experienced abuse and repetitive mTBI. These children also require an individualized treatment plan for their overall recovery. As we continue to learn more about recovery from brain injury, we will be able to discern whether brain injury–induced symptoms will need to be treated differently than conditions attributed to trauma or idiopathic diagnoses. Until then, ensuring that these children receive proper pharmacologic and non-pharmacologic care is crucial to help them meet developmental milestones. Survivors of child abuse and repetitive mTBI must be able to obtain treatment for any prolonged cognitive, behavioral, or affective symptoms that interfere with the activities of daily life. By doing so, these children are given the opportunity to improve their quality of life as they reengage life at home, in school, and throughout society as children and into adulthood. Joshua A. Beitchman: Conceptualization; writing—original draft; writing—review and editing. Suzanne Dakil: Conceptualization; supervision; validation; writing—review and editing. Mathew Stokes: Conceptualization; resources; supervision; validation; writing—review and editing. The authors declare no conflicts of interest.