Further recommendations of the International Paediatric Brain Injury Society (IPBIS) for the post-acute rehabilitation of children with acquired brain injury

ABSTRACT

Background

Paediatric acquired brain injury is a life-long condition which impacts on all facets of the individual’s lived experience. The existing evidence base continues to expand and new fields of enquiry are established as clinicians and researchers uncover the extent of these impacts.

Primary objective

To add to recommendations described in the International Paediatric Brain Injury Society’s 2016 paper on post-acute care for children with acquired brain injury and highlight new areas of enquiry.

Review of information

Recommendations were made based on the opinions of a group of experienced international clinicians and researchers who are current or past members of the board of directors of the International Paediatric Brain Injury Society. The importance of each recommendation was agreed upon by means of group consensus.

Outcomes

This update gives new consideration to areas of study including injuries which occur in pre-school children, young people in the military, medical referral, young offenders and the use of technology in rehabilitation.

KEYWORDS:

• Children
• traumatic brain injury
• advocacy
• health
• recommendations
• acquired brain injury
• young people

Introduction

In 2016, the International Paediatric Brain Injury Society (IPBIS) published its first series of recommendations on the post-acute care of children with acquired brain injury (ABI) (1). These recommendations were built on a number of consultations with international experts in the field spanning twelve years. These recommendations proposed development of an international service provision model to address the needs of the child and family in a holistic fashion across the entire spectrum of ABI. Acknowledging that care is often fragmented and limited following discharge from medical services, fourteen specific practice recommendations and action plans were generated across three core areas: 1) medical and rehabilitation, 2) family and education, and 3) cognitive and behavioral. These recommendations encompassed increasing educational competence, communication, and collaboration across medical, rehabilitation, and educational systems of care; addressing children’s long-term health, cognitive, behavioral, and educational needs, particularly at key developmental transitions; and providing family-centered care and interventions. Special additional areas of consideration were recognition and management of concussion and ABI in the developing world. Seven years later, the field of pediatric brain injury has continued to develop with greater consideration given to new and important fields of study. Our first set of recommendations, while still relevant, have now been expanded, based on the expertise of members of the IPBIS board of directors. These further recommendations are based on the opinions of ten members of the IPBIS board of directors and their importance to the field were agreed upon by group consensus. These experts come from the fields of medicine, psychology, education, and rehabilitation and represent viewpoints from seven countries.

For the purposes of this article, we have defined ABI as any injury to the brain which has occurred following birth. These include diseases of the brain, stroke, infection, hypoxia or trauma. Much of the research cited below relates specifically to ABI caused by trauma and will be referred to as traumatic brain injury (TBI). We use the term ABI to encompass an area where the evidence base includes injuries caused by both traumatic and non-traumatic means. We do not focus on any particular level of severity in this manuscript and draw from research focusing on mild to moderate and severe injuries. We use the term pediatric to refer to children and young people between the ages of 0–24 years due to the stages of brain maturation which are thought to complete by the mid-20s (2).

Special considerations for the preschool population

Of all ABIs, TBI occurs most frequently in children under the age of 6 years (3). The estimated annual incidence of TBI requiring hospitalization in New Zealand, Australia, Europe and the United States varies between 60–250 per 100,000, with 80–90% of these cases classified as being mild (4–6). A recent study reported a peak incidence rate for children aged 0–1 year that was 100 times that of the overall incidence rate (7). Due to the large number of children affected by these injuries, any persisting developmental consequences are of significance and likely to impact on the developmental course of the child.

Early childhood is characterized by maturation of physical, cognitive and social skills. This is particularly relevant for children aged 0–5 years who are still developing basic motor skills. It is therefore not surprising that falls are the leading mode of injury, with the majority of these injuries occurring in the home (4,8,9). Cognitive and social skills are also rapidly developing during childhood and are associated with major changes to neural networks (10,11). Recovery trajectories associated with TBI will be affected by developmental changes, with emerging or undeveloped skills being considered more vulnerable to TBI than previously established skills, because of the potential for disruption to the networks that mediate the development of these skills (12). For example, Keenan et al. (13). reported that preschool children with severe TBI evidenced deficits in communication, gross motor skills, problem solving and social domains 12 months post-injury. However, these outcomes differed by age at injury, with younger children evidencing more difficulties than older children. Long-term functional academic skills were lower in those injured as infants and preschoolers than in those injured as older children and adolescents, again suggesting vulnerability of young children to less favorable attainment of core developmental skills (14). Children who sustain their injury after learning academic skills find them easier to reacquire compared to those injured before such skills have been learned (14). Longitudinal studies suggest that while these skills can improve in the first 6–12 months following injury, deficits in these skills persist from between 1–5 years after injury (15,16). While new skills will continue to be learned, children with TBI continue to lag behind their typically developing peers (14). Finally, due to the unique characteristics of the social and family environment during early childhood, there is reason to pay particular attention to the effects of TBI on parent-child relations and family functioning more broadly (17–19).

While the TBI literature on the preschool population is less extensive than for school age children, it has identified similar problems including deficits in social competence (20), internalizing and externalizing behaviors (21), sleep problems (22), Verbal IQ, receptive language and reading comprehension (23), increased rates of academic problems on entry to school (24), Attention Deficit Hyperactivity Disorder (25), gross motor skill and problem solving deficits (13). Recent scoping and systematic reviews conclude that children who experience a TBI before 6 years of age are at risk for persistent long-term difficulties in cognitive, academic and social functioning (26,27), supporting previous work suggesting that even a mild TBI in early childhood can result in long-term deficits in behavior that can persist into adulthood (28,29).

Despite the evidence that early brain injury can be associated with persisting problems, there are a number of unique challenges in identifying and providing appropriate input for children who experience an early TBI. Arguably the most important challenge is identifying that the injury has occurred, followed by a need to ensure the provision of appropriate follow-up. For most children under the age of 5 years, the TBI is likely to be mild, and will depend on an adult recognizing that the injury has taken place and presenting them to an emergency department for evaluation. Moreover, the youngest children are pre-verbal and rely on adults identifying any symptoms. Research indicates that parents report significantly fewer symptoms for younger children with mild brain injury than for school-aged children (30); however, this observation may be associated with methodological limitations in symptom reporting at this age as noted in recent work proposing a developmentally-appropriate observational approach to symptom identification (31). Preschool children are also less likely to have imaging due to clinical decision-making guidelines to restrict CT radiation exposure and challenges associated with obtaining neuroimaging in research contexts, with one study reporting that only 2.3% of children under 5 years of age underwent CT scanning compared to 8.8% of adolescents (32). As such, there is limited information on the nature and extent of how an injury can impact on brain structure and function in this group. Additionally, a recent review of the literature for preschool children reported that they are less likely to experience loss of consciousness, and other markers, such as length of post-traumatic amnesia, are difficult to assess in this population (33). Further, regardless of brain injury severity, preschool children are less likely than older children to be admitted to hospital, rather discharged to home without any referral to follow-up services, resulting in early rehabilitation not being provided (34).

Preschool children are vulnerable to not receiving appropriate services to assist them in their rehabilitation as there is often no information about their pre-injury ability, and they are still at the early stage of development. For preschool children, educational accommodations are rarely made (34). When children experience ABI they are likely to require assistance, however, a recent study reported that, regardless of severity, when these children reach primary school most of their needs will remain unmet (24).

Actions

There is an urgent need for a clear pathway of care for children who experience a brain injury event during the 0–5 year period, as these children may have unique unmet needs. This should include the development of more appropriate measures to identify brain injury at the point of injury. Further, when a child is discharged, parents should be provided with information about the effect of TBI on the development and learning needs of their child. Preschools need to be informed and make appropriate accommodations to meet the needs of these children. Information about the injury should also be communicated to educators when the child transitions to primary school so that appropriate accommodations can be made and support provided. Importantly, there needs to be a greater understanding of the ongoing needs of children who have sustained a preschool TBI. Given the often unpredictable course of recovery, the future development of children who sustained a TBI of any severity during their preschool years should be monitored across healthcare and educational settings, especially at developmental transition points.

Medical referral to follow-up and rehabilitation after ABI

National medical recommendations for when to follow-up and refer to rehabilitation after pediatric ABI are rare (35–37) or minimally described (38). Development of guidelines for the rehabilitation of pediatric ABI are complicated by the heterogeneity of diagnostic categories and medical interventions. For example, for patients with brain tumors, the medical treatment with surgery, radiation and/or chemotherapy affects cognitive outcome in a way that differs from other diagnoses of ABI. Even within subgroups of ABI, symptoms are heterogeneous and differ widely in severity. Numerous studies characterize the impact of ABI on outcomes in children with diverse diagnoses, including TBI (39–41), encephalitis (42), stroke (43,44) and brain tumors (45–47) Outcome is also influenced by the age at injury, with younger age at injury being connected to poorer outcome after TBI (48) and brain tumors (49), as well as ABI in general (18). Another aspect is that time after injury influences outcome, with older age at injury being connected to faster recovery after ABI (18). Also, possibilities for neurocognitive recovery is strongest within two years after TBI (41) and encephalitis (50). After this, improvement of deficits is slower and with the risk of dysfunctions remaining permanent (41,50) while functional improvements in everyday life can still be achieved by effective coping strategies (51). Thus, recommendations for referral to ongoing support after ABI must be adapted to the etiological diagnosis, the different levels of severity, age at injury and time since injury.

Emergency care physicians treating children with TBI have expertise in acute treatment, but are seldom experienced in the follow-up and rehabilitation of these patients. This is also the case for primary care physicians who are often the first point of contact for children with mild TBI (52), pediatric oncologists and pediatricians treating CNS infections. During the acute stage, it is also often hard to know who will experience long-term difficulties. Among patients who have sustained a TBI, more than 80% have mild injuries (53,54). While most of those with mild injuries recover and return to school within a month, some children experience long-lasting difficulties (55), for example with headache, vestibular dysfunction, fatigue and difficulties with memory. There is also an increased risk of attention deficit/hyperactivity disorder and conduct disorder (54). Pre-morbid factors and cognitive consequences of the injury that pose a risk for persisting cognitive symptoms may not be immediately visible. There is a risk that these factors will not be investigated and treated properly as the often more obvious movement-related symptoms. Patients who have sustained a severe ABI are often treated in specialized health care units. However, recommendations are still lacking about how to follow-up deficits and when to refer to long-term rehabilitation. Factors affecting the rate of referral may be caused by lack of knowledge about the implications of pediatric ABI, or lack of healthcare resources, including rehabilitation services. There may exist healthcare services providing initial stages of rehabilitation while those providing long-term rehabilitation services after discharge from hospital may be few. As the school system is tasked with caring for children returning to school across the spectrum of ABI severity, establishing formal systems of continuity of care from medical to educational settings is critically important. Such systems should include best practices for educating educators and managing returning to learning (56).

Actions

International and/or more specific national evidence-based recommendations are required concerning follow-up after ABI. These recommendations should include how to assess symptoms after different causes and severity of pediatric ABI. They should have a special focus on how to assess cognitive, communication, and emotional deficits. Planning of follow-up should be made with regard to age at injury and time since injury. Recommendations should include information on individual pre-injury and social factors increasing the risk for persisting problems and hence guiding the need for follow-up. Also, they should give guidance on indicators for a range of service options including when to refer to a specialized rehabilitation unit, or to community rehabilitation services, to school supports, or for other interventions. The importance of written information should also be stressed. Written materials should include common symptoms, methods of managing symptoms, supports, and methods of preventing reinjury. It should hold information of common symptoms, how to minimize them and how to prevent a new injury to the brain. The information should include recommendations about how and when to return to activities and school and should be forwarded to teachers and trainers. It is also important to include advice on where to reach support services, if symptoms last longer than four to six weeks.

Parents should also be informed about the availability of rehabilitation services for their child so they can better make informed decisions about their care. It is important to manage the expectations of parents for their child’s rehabilitation, providing them with realistic goals which will hopefully be exceeded. Finally, the availability of long-term services for ongoing deficits after ABI needs a special focus in healthcare and educational planning.

To advance the evidence base that is the foundation of these recommendations, future research should test specific intervention components that are hypothesized to impact carefully defined outcomes. The Rehabilitation Treatment Specification System (57) is an example of a strategy to characterize specific ingredients and targets. This approach has potential to accelerate the development of validated approaches to rehabilitation and clarify which treatment components work for which outcomes for children presenting with specific symptoms.

Use of technology in pediatric rehabilitation

Technology use in rehabilitation following ABI can broadly be divided into approaches which are intended to restore or compensate for reduced functioning. The use of technology to offer support and rehabilitation to children and young people following brain injury offers great potential. This potential arises due to issues of scale whereby a technology may support many times the numbers of patients when compared to a single clinician. This also potentially means that the cost of rehabilitation can be reduced and patients can receive care in a timely fashion (58). Some existing technology-based interventions make use of telemedicine to allow for the delivery of rehabilitation in the patient’s home (59,60) which may also have the advantage of increasing engagement and is certainly more convenient.

The development of new approaches to using technology in rehabilitation is an exciting and ongoing area of work. Researchers have created online training resources (61), made use of paging devices (62), text messaging (63), apps (64,65), electronic calendars (66), voice recorders (67) and robotics (68). However, research is at times hampered by small-scale studies which employ either single-case designs or have limited numbers of participants. There are few large scale, robust, randomized controlled trials which provide clear evidence of the effectiveness of these approaches. However, Wade and colleagues (60) utilized a RCT methodology to test their online problem solving intervention for adolescents with executive functioning deficits, showing that those with severe TBI made significant improvements when compared to a matched control group using widely available internet resources. Bangirana et al. (69). utilized computerized cognitive rehabilitation training in a RCT to improve memory, learning, psychomotor speed and internalizing behavior in children who suffered from ABI (69). Only learning showed a statistically significant improvement for the intervention group (69). It is important for researchers to take forward promising interventions to trial status to ensure we have the best available evidence before introducing such programmes into the clinical setting.

During the COVID-19 pandemic many services and rehabilitation efforts have been forced to move to online delivery. The rush to deliver virtual healthcare has been a global phenomenon which showed the potential to increase online contact with clinicians (70). As clinicians and patients became more familiar with this approach, and some regulatory barriers were removed, delivery of care was transformed (71). Whilst it was not possible for all services to proceed in this manner, dedicated clinicians readily took up the challenge and adapted their practice accordingly. However, clinicians have warned that while there are many benefits of online healthcare this cannot entirely replace the more traditional physical examination (71), or indeed the therapeutic relationship. Patient preference, trust and reassurance must also be taken into consideration in the delivery of therapeutic interventions which employ technology. The growing sophistication of digital media consumption by patients means that technology can quickly grow stale and outdated. It is therefore crucial to offer patients engaging, relevant content which directly speaks to their experiences and needs. Some populations may also have poor access to technology, be uncomfortable with its use, or lack adequate internet coverage, creating disadvantage in delivery of such programmes (58).

Actions

Increase collaboration between researchers to encourage large-scale multi-center trials of promising technology-based interventions. These will ensure delivery of high quality evidence in regard to efficacy. Researchers and clinicians should co-develop such interventions with survivors of brain injury and their families to ensure these address their needs and will be utilized beyond the development and research phases. Technology-based interventions should face periodical review to ensure they are current and up to date to better offer patients an engaging experience. Clinicians should ensure their patients have adequate training in and access to technology when seeking to engage them with services or treatments which utilize such approaches.

TBI among military personnel

The age at which young people are accepted for military service varies around the world and ranges from age 16 to 20 years with most countries recruiting around ages 17/18 years. The US Central Intelligence Agency (CIA) lists the minimum age of voluntary or mandatory military service for all countries (72). Consequently, there are considerable numbers of young people in the military, often placed in conflict situations, whose brains are still developing and thus are at particular risk of significant injury.

Recent military conflicts have raised awareness of the high prevalence of TBI among young service personnel. The incidence of TBI arising from the Afghanistan and Iraq wars has been well studied, and the incidence of poor mental health conditions associated with mild or moderate TBI has been reported as affecting up to 320,000 service members (73).

Military service personnel are at risk of both blunt and penetrating brain injury in the combat environment and even in peacetime are at greater risk of TBI when compared to civilian populations (74). They are also at risk of long-term cognitive and mental health problems. Armed forces mostly comprise young men. In a retrospective cohort study of 4980 critically injured U.S. military service personnel during combat operations in Afghanistan and Iraq, the average age was 25.5 years and 98% were male (75). This indicates that many personnel suffered TBI within a period of increased vulnerability when their brains are still developing. The study found that almost one third had moderate to severe TBI. Of the 4980, the majority (71%) were diagnosed with at least one mental health condition, and TBI was associated with an increased number of mental health diagnoses. Over half of those with TBI had been diagnosed with post-traumatic stress disorder (PTSD) (75).

A study of 2440 UK casualties among service personnel in Afghanistan and Iraq found that 19% were recorded as sustaining TBI, mostly moderate or severe (76). Injuries caused by Improvised Explosive Devices (IEDs) accounted for approximately half the TBIs. IEDs can cause multiple and complex injuries including those from primary blast injuries (explosive forces) and secondary blast injuries caused by projectiles from within the bomb. These have the potential to cause TBI. However, it was noted that other significant injuries resulting from an IED could mask the presence of mild TBI, so that TBI may be under-recorded. It is concerning that almost half the TBI survivors did not receive neurorehabilitation.

The long-term consequences of TBI among ex-service personnel may persist for years post-TBI. Once service personnel leave the military they can struggle to cope and find the support they need and they are often reluctant to ask for help. Studies have found that ex-military personnel post-TBI have unmet service needs, particularly concerning support for cognitive and emotional issues and vocational skills (77).

Actions

Improve ways of recognizing and identifying TBI, particularly where mild TBI may be missed due to significant other injuries. Routine screening for mild TBI is advised for service personnel returning from active duty, suitable brain injury screening tools are available and are used by some countries but not all. Service personnel should be monitored post-TBI, particularly when they have left the military and are at risk of being lost to follow-up. Promote the use of online resources offering advice and support for veterans post-TBI, for example Real Warriors, a programme through the Defense Centers of Excellence for Psychological Health and Traumatic Brain Injury (DCoE), provides information and resources about psychological health, TBI, and PTSD (78). In the UK, Combat Stress provides support and self-help guides for veterans from every service and conflict, particularly those with anxiety, depression or complex mental health issues (79).

Recognition of ABI and intervention with offender populations

It is now recognized that the prevalence of ABI among offender populations is many times that of the general population (80–82). Research suggests that these figures may be anywhere between 16% (83) to 87% (82) compared to approximately 8.5% in the general population (84). Offenders, particularly young offenders, comprise a vulnerable population who possess a range of co-morbidities and disadvantages which can complicate their rehabilitation trajectory (85,86). Offenders are more likely to come from economically deprived areas, suffer from substance misuse problems, poor mental health, low levels of education and may have been victims of abuse (54,87,88)

One of the greatest barriers to supporting offenders is the lack of recognition and understanding of ABI by members of the criminal justice system (CJS) (89,90). For example, young offenders with frontal lobe dysfunction may exhibit deficits in planning, initiation and inhibition and may have difficulty in identifying social cues necessary for empathic response (90,91). This could be interpreted by members of the CJS as the young person being uncaring, disorganized and apathetic which could lead to the formation of negative judgments about their sentencing and future prospects.

Given demands placed on public resources, there may also be a perception that supporting offenders does not provide value for money. However, figures from the UK suggest that the long-term cost of young offenders with head injuries to the taxpayer is £345,000 (92) (approximately $460,000 US). This is in contrast to a young person with TBI who had committed no offense (£94,000 or $125,000 US) (92). Clearly, programmes which are successful in diverting young people from criminal activities will have a significant impact on reducing such costs. However, there is a dearth of research on interventions for ABI, which take into consideration the range of co-morbidities, of young offenders.

Actions

Increase screening of ABI among young offender populations across the CJS. Increase understanding among professionals within the CJS at all levels. An existing resource provides information, descriptions and strategies for those delivering psycho-educational programmes to adolescents and young adults with ABI within the CJS (93). This, together with other approaches (e.g. sport, art, vocational activities), could be used to create tailor-made interventions which take into consideration the unique circumstances in which young people with ABI involved with the CJS are situated.

Paediatric TBI in low and middle income countries (LMIC)

The WHO has reported that road traffic injuries are the leading cause of death in children and young adults aged 5–29 years (94). Around 93% of the world’s fatalities on roads occur in LMIC, where more than 85% of the world’s population live (94). A recent systematic review has shown that 39% (n = 16,275/41,979) of all TBIs in children are caused by road traffic accidents in LMIC (95).

More than half of all road traffic deaths in LMIC occur to the most vulnerable road users namely pedestrians, cyclists, and motorcyclists (94). Correct use of helmets on two wheeled vehicles, and child restraints in cars, are thought to reduce the risk of death by 42% and 60%, respectively; however, there is poor compliance of these essential road safety measures in many LMIC (96). While these measures should reduce risk of death, less is known about their impact on TBI, which is largely due to lack of implementation and good quality data on the epidemiology of TBI in LMIC (95,97).

Evidence suggests that access to early treatment for TBI, crucial for improved outcomes, is poor for people living in LMIC (33% within 6 h) (97) when compared to high income regions (80% within 1 h) (98). At the time of discharge from acute care, 25% to 50% of children and young adult TBI patients in LMIC still have some physical, cognitive, or behavioral deficit leading to poor quality of life (95,99). However, access to rehabilitation services in LMIC for people with disabilities is poor (100).

Actions

There is urgent need for further, high quality evidence on the epidemiology of TBI in LMIC, without which governments will fail to act. A large-scale international collaborative effort is required to collect data on the epidemiology of TBI in LMIC and develop guidelines for its management whilst being mindful of the limited resources available in these countries. Legislators in LMIC should give priority to preventing TBI in children by enforcing the wearing of helmets on two wheeled vehicles, use of child restraints in cars and creating safer roads for children. Governments of LMIC should create facilities for neurorehabilitation and provide outreach services to address the unmet needs of children and young people with TBI, allowing them to attend school or gain meaningful employment.

Conclusions

Many of the recommended actions included in this paper call for more education and awareness of ABI across a range of populations. From pre-school to young offenders and military personnel, the need for improved identification of injury and development of care pathways is a clear concern. Greater recognition that brain maturation may not reveal deficits for many years is needed to ensure that adequate monitoring and appropriate care are in place across the developmental trajectory. As clinicians and researchers in pediatric brain injury, we have an important role to play in advocating for services and policies which better meet the needs of these vulnerable individuals and their families. It would also be important to support families in becoming self-advocates in the care of their family members. As children are dependent on the family, increased recognition of the influence of parents on their child’s clinical course is needed. Rehabilitation programs should also provide supports for family functioning, including parent psychological health, along with parent coping skills and parenting strategies, that positively impact children’s well-being. Parents often refer to the struggle to receive appropriate services, and we as professionals should be better at supporting them in achieving this goal. It is worth noting that the IPBIS has created a freely available toolbox (http://toolbox.ipbis.org/) which captures a number of useful interventions and resources intended to support families and the work of professionals.

In addition to the developmental concerns noted above, there are barriers to implementation of these recommendations that will vary across international systems of care. There are several core areas that should be targeted to enhance service delivery. It is essential to improve healthcare policy and funding to support children and their families. To address fragmentation of knowledge and services, best practices need to be validated and scaled up across institutional boundaries. It is critically important that the integration of such community systems encourages diffusion across settings from specialty acute care and rehabilitation to primary care and community providers as well as to education, justice, and military systems.

The IPBIS hope to continue to update these recommendations as the field of pediatric brain injury continues to grow and develop. We would welcome contributions from other researchers and experts for future publications. Additional topics of concern that should be addressed in future articles include disorders of consciousness, intimate partner violence, and abusive head trauma. Systems of support to cover the full range of needs of children with ABI across developmental transitions are an essential area to target. We hope that by highlighting some of these issues and suggested actions, a road map for future collaborative working can be developed.

Ethics statement

As this manuscript did not include data collection it was exempt from ethical approval.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Correction Statement

This article has been republished with minor changes. These changes do not impact the academic content of the article.