RESEARCH IN CONTEXT

Neuropsychological and cognitive outcomes are best described for relatively homogeneous, high-risk populations of PICU survivors (such as cardiac arrest and traumatic brain injury), but less is known about the PICU survivor population overall. When performed, detailed neuropsychological evaluation in a PICU population at risk for neurologic injury demonstrates post-PICU deficits in intelligence quotient and executive function, such as working and spatial memory and attention. An abbreviated neuropsychological and cognitive screening protocol that identifies the common cognitive challenges of PICU survivors with acquired brain injury may provide a time-effective means to evaluate larger survivor populations and expand our understanding of outcomes after critical illness in childhood.

AT THE BEDSIDE

In our programs, abbreviated neurocognitive and psychological evaluation of PICU survivors with primary or secondary brain injury successfully identified the same deficits commonly found among PICU survivors who undergo longer, more complete testing protocols. A focused neuropsychological evaluation that can be completed in less than an hour can effectively and efficiently identify enough cognitive performance information to guide many practical recommendations to improve PICU survivors’ return to school.

Recent estimates indicate that nearly 250,000 children are admitted annually to an ICU in the United States (1,2). In dedicated PICUs, a substantial proportion of these admissions are associated with complex multisystem disease, advanced technological support, and risk of significant morbidity and mortality (3). Over the past 3 decades, mortality in children admitted to the PICU has steadily decreased, with recent studies reporting an overall 2% mortality among children admitted to the PICU (4). This improvement in survivorship has led to a burgeoning field of research exploring post-ICU outcomes (5–9). Of particular interest is the relationship between both primary and secondary neurologic injury and cognition, as there is now a significant body of research demonstrating that survivors of critical illness in childhood are susceptible to lasting cognitive effects that distinguish them from their healthy peers (10–12). Recent data indicate that these cognitive changes typically manifest in areas regulated by the executive functioning system such as working memory, spatial memory, and information processing (13,14). The functional consequences of these findings are often academic, as teachers frequently identify PICU survivors as having problems with school work and performing below average in the areas of executive function and attention (15). In some cases, these academic problems persist for years after PICU discharge (16).

Traditional neuropsychological evaluation for children encompasses multiple domains of cognition, including but not limited to intelligence, problem-solving, executive functioning, memory, language processing, visuospatial functioning, physical dexterity, academic skills, behavior, and social skills. A complete neuropsychological battery typically requires four or more hours for completion. While this approach is unquestionably thorough, it has some practical limitations for PICU follow-up programs hoping to establish timely neuropsychological evaluations and support for children before they return back to school. However, a more targeted neuropsychological evaluation can focus on the deficits most often found in PICU survivors, include assessments that identify major areas of concern for school performance, and still be completed in under an hour. When combined with services targeted to successfully reintegrate PICU survivors back to school, this more focused evaluation could provide an effective and efficient means of screening for cognitive deficits among PICU survivors and provide a rationale for early academic support (even if it is temporary as the child continues to recover) upon the child’s return to school.

The Pediatric Neurocritical Follow-up Program at St. Louis Children’s Hospital and the Pediatric Critical Care and Neurotrauma Recovery Program at Doernbecher Children’s Hospital were established on the foundational belief that cognition is an essential outcome for PICU survivors, and our common programmatic goals have been to facilitate the successful return of our patients back to their social and academic lives. For more than 5 years, our multiprofessional teams have performed targeted neuropsychological screening evaluations for children with acquired primary or secondary brain injury and assisted their families with the implementation of our recommendations for new accommodations at school. At the time our programs began, we hypothesized that our approach of targeted evaluation would successfully identify children with neurocognitive deficits and psychological concerns. Herein, we report the pooled results of our approaches, including details of our testing battery and our teams’ process for returning our patients back to school.

MATERIALS AND METHODS Program Structures

St. Louis Children’s Hospital is a 250-bed tertiary children’s hospital within the Washington University School of Medicine, located in St. Louis, Missouri. The PICU has approximately 2,200 admissions per year. Doernbecher Children’s Hospital is a 145-bed tertiary children’s hospital within Oregon Health & Science University located in Portland, Oregon, with approximately 1,300 admissions to the PICU annually. In both institutions, the multiprofessional neurocritical care follow-up teams are composed of faculty in Pediatric Critical Care, Pediatric Neurology, and Pediatric Neuropsychology, with the addition of mental health and school liaison services at Washington University. Patients with newly acquired primary or secondary brain injury are eligible for inclusion in the programs, the details of which are published elsewhere (10,17–19). PICU families are introduced to our teams during their inpatient stay, and at hospital discharge, participating families are scheduled for outpatient neurocritical care follow-up roughly 4 weeks later. At the follow-up appointment, each child receives: 1) full neurologic and physical evaluations; 2) individual or parent/caregiver proxy screening for problems with sleep quality, mood, functional status, and health-related quality of life; and 3) a targeted, age-appropriate developmental or neurocognitive assessment.

The Pediatric Critical Care and Neurotrauma Recovery Program in Portland were established under Institutional Review Board (IRB) approval at Oregon Health & Sciences University (No. 16173, August 4, 2016) for clinical care and research activity. This research was deemed to be within the scope of this IRB protocol and was performed in accordance with the Helsinki Declaration of 1975. Because it included only secondary analysis of existing data, the requirement for informed consent was waived. The Washington University IRB also approved this protocol as secondary analysis of existing data and also waived the requirement for informed consent. This study is presented in a format consistent with the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines for reporting cohort studies (http://www.equator-network.org/).

Connection With the Neurocritical Care Teams During the Inpatient Stay

Connection with both neurocritical care follow-up programs begins while the child is still in the hospital. In Portland, the lead neuropsychologist sits down with parents/caregivers to: 1) establish care by introducing the family to the follow-up program; 2) address any acute recovery needs related to post-intensive care syndrome (PICS) that the inpatient treatment team identifies as a concern; and 3) conduct an interview focused on pre-hospitalization levels of functioning. The team’s neuropsychologist continues to meet with the child and family during the hospital stay to provide psychological support and helps to coordinate the first follow-up appointment at the time of discharge. In St. Louis, connection with families begins with the team nurse to provide PICS education and present the goals of the program. In 2019, the St. Louis team added a school liaison to ensure that the recommendations made by the neuropsychologist could be effectively implemented at school. Since then, the school liaison also meets with families during their inpatient stay to review the child’s baseline academic performance and any academic accommodations that were in place prior to PICU admission. A full listing of our teams’ composition is shown in Table 1.

TABLE 1. - Composition of the Neurocritical Care Follow-Up Programs Role Clinical FTE Description of Clinical and Nonclinical Duties Pediatric intensivist 0.1–0.2 Program management, development and implementation of new program initiatives, personnel hiring and oversight, development of educational curricula, oversight of research activity and publications, direct patient care (S, P) Pediatric neurologist No dedicated program timea Outpatient evaluation and management (S, as needed P), participates in bimonthly team meetings and other program activities (S) Pediatric neuropsychologist 0.4–2.0 Initial inpatient evaluation and consultation (P), outpatient evaluation and management (S, P), liaison for school supports (P), psychology treatment clinic (P) Program manager 0.3 Program management, development and implementation of new program initiatives, personnel hiring and oversight, organization of bimonthly team meetings, annual program performance evaluation and documentation (S) Nurse coordinator 0.5 Inpatient family education and enrollment into the program, longitudinal inpatient follow-up, maintains active program patient list, schedules program appointments, participates in bimonthly team meetings and other program activities (S) School liaison 0.5 Inpatient family education and child educational assessment, participates in neuropsychologist feedback sessions and follow-up with families and schools as indicated, participates in bimonthly team meetings and other program activities (S) Neurology nurse 0.2 Schedules patient appointments, performs screening phone calls and associated documentation prior to clinic appointment, participates in bimonthly team meetings and other program activities (S) Social work 0.1 Family support and resource provision (e.g., transportation) as indicated by team (P)

FTE = full-time equivalent, P = Portland program, S = St. Louis program.

aPediatric neurologist clinical time for each program is included in total outpatient neurology clinical FTE calculation per each faculty member’s contract.

Duties as performed by team members in the P and S.

Outpatient Follow-Up Appointment Medical Evaluation

At the follow-up visit, each child completes a 30- to 40-minute appointment with our teams’ medical and/or neurology providers. This includes completion of a packet of outcome measures from the National Institute of Health’s Patient-Reported Outcomes Measure Information System (http://commonfund.nih.promis) assessing recent mental health symptoms, symptoms of pain or fatigue; the Pediatric Quality of Life Inventory (https://pedsql.org) assessing family functioning; and the Sleep Disturbance Scale for Children or Brief Infant Sleep Questionnaire to assess recent sleep quality (20,21). Packets are completed by the children and/or their parents/caregivers, dependent on age, and when possible, families are encouraged to complete them in advance of clinic via an online interface. In clinic, children and their parents/caregivers also complete a standardized review of recent medical history; current medications; and a thorough physical and neurologic examination. During the appointment, the outcomes measures from the packet are scored, and any identified concerns are reviewed with the children and parents/caregivers.

Neurocognitive and Psychological Evaluation

Both programs also invite all school-aged children to undergo a screening neuropsychological assessment in a quiet, reduced-distraction, 1:1 medical setting (In Portland, infants, toddlers, and young adults are also invited to undergo evaluation, but data from these participants is not included in this report). Administration time for the neuropsychological assessment takes anywhere from 30 to 45 minutes, depending on the patient’s age, level of ability, cooperation, and the impact of their medical history (Supplemental Table 2, https://links.lww.com/PCC/C395).

At the outpatient visit in Portland, patients also receive an age-appropriate, brief neuropsychological or developmental evaluation by the team’s lead pediatric neuropsychologist. The neuropsychologist then sits down with the family to explain the results of the evaluation and interpret the findings. Referrals are made in real-time time as indicated (e.g., other medical specialties; rehabilitation services; the long-term recovery neuropsychological assessment clinic; social work; the family-focused psychology PICS treatment clinic; the family support group; and/or other community-based programs). If applicable, a release of information is signed that grants the team permission to connect the family with the Oregon Department of Education’s Traumatic Brain Injury Liaison team to help establish a relational bridge between the follow-up program and the child’s school district in order to coordinate and develop a reintegration strategy and a plan for long-term support.

At the follow-up appointment in St. Louis, families first sit down with the neuropsychologist and school liaison to review their child’s complete medical history and PICU course, recent parent concerns, and questions about testing. The child then meets individually with the neuropsychologist while the family completes an executive function questionnaire (the Behavior Rating Inventory of Executive Function, Version 2 [22]) in the waiting room. Once the child’s evaluation is completed, the results are scored, and the neuropsychologist sits down with the family and the school liaison to explain the results and interpret the findings. Follow-up plans for repeat testing in the future and/or communication with school are made at that time. The school liaison maintains communication with the patient and family to coordinate reintegration planning, arrange remote learning, or arrange formalized homebound instruction until the child can safely transition back into in-person school attendance.

Neurocognitive and Psychological Testing Protocol

The content and duration of neuropsychological testing varies slightly between our institutions, based on provider preference and availability of testing instruments. Briefly, all patients greater than 4 years old undergo a series of screening tests to evaluate attention and working memory (16 min), visual processing (3 min), verbal fluency and processing speed (13 min), auditory learning (7 min), and coordination (5 min) for review (Supplemental Table 3, https://links.lww.com/PCC/C395). Additional tests may be added for specific pathology/location of injury. Neurocognitive impairment is generally defined by scores on individual assessments within each domain that are more than 1.5 sds below standardized population means (e.g., standard scores < 78 and scaled scores < 6). Consistent with prior work, anxiety, depression, and cognitive concerns are recorded for T-scores greater than 55 indicating moderate or severe symptoms (23–25).

Although the St. Louis program sees patients for one visit only after hospital discharge, the Portland program is longitudinal and retains patients for clinical follow-up for as long as needed after they discharge from the hospital. Data presented here are from all appointments in St. Louis and only the first appointment in the Portland program to ensure that all data were reflective of patient and parent experience and health status at roughly 1 month post-hospital discharge. For ease of reporting, all results were summarized using standard classifications of neurocognitive diagnosis or recommendation and are presented as integers and percent of each institution’s population.

RESULTS Follow-Up Program Populations

Between 2017 and 2021, our combined institutions performed 289 targeted neuropsychological evaluations for PICU survivors greater than 4 years old (Table 2). More than half of evaluated children were greater than 10 years old, and most were male. Traumatic brain injury (TBI) was the most common diagnosis for program participants in both institutions, but mild TBI patients were far more likely to meet inclusion criteria in Portland than in St. Louis (Supplemental Table 1, https://links.lww.com/PCC/C395). Relative differences in areas of clinical focus and follow-up strategies resulted in other population differences as well, including a higher proportion of COVID-19/multisystem inflammatory syndrome in children patients in the Portland program (11% vs 3%) and a higher proportion of pediatric stroke patients (31% vs 6%) and extracorporeal membrane oxygenation patients (14% vs 1%) in St. Louis. These differences in patient populations also resulted in differences in the proportion of patients in the follow-up programs receiving mechanical ventilator support and the overall hospital length of stay (Supplemental Table 1, https://links.lww.com/PCC/C395). At the time of their first follow-up appointment, more than three-quarters of patients at both institutions had returned to school (Table 3).

TABLE 2. - Follow-Up Program Patient Characteristics Variable Total Population (n = 289) Patient age, yr, median (IQR) 13 (9–16) Patient age group, n (%)  5–10 yr 97 (34)  11–15 yr 117 (41)  > 15 yr 75 (26) Male sex assigned at birth, n (%) 169 (58) Race, n (%)  White 199 (69)  African American 28 (10)  More than one race 13 (4)  Other race 18 (6)  Not reported 31 (11) Hispanic ethnicity, n (%) 27 (9) Insurance status, n (%)  Medicaid 155 (54)  Private 119 (41)  Other or uninsured 15 (5) Patient diagnoses, n (%)  Traumatic brain injury   Mild 117 (40)   Moderate/severe 59 (20)  Stroke/arteriovenous malformation 43 (15)  Infectious/inflammatory 16 (6)  Status epilepticus 4 (1)  Extracorporeal membrane oxygenation 16 (6)  Respiratory failure with hypoxia 5 (2)  COVID-19/multisystem inflammatory syndrome in children 18 (6)  Other 11 (4) Pre-hospital chronic conditions, n (%)  Medical 69 (24)  Psychiatric 51 (18)  Neurodevelopmental 67 (23) Hospitalization characteristics  Hospital length of stay, d, median (IQR) 11 (4–27)  Intubation, n (%) 160 (55)

IQR = interquartile range.

TABLE 3. - Results of Neuropsychological Testing Variable Total Population (n = 289) Back to school at time of clinic, n (%)  Not back to school 55 (19)  Returned part-time 22 (8)  Returned full-time 182 (63)  N/A (e.g., summer break) 31 (11) Parents of patient report cognitive concernsa, n (%) 72 (25) Parents or patient report emotional/behavioral concernsa, n (%) 140 (48) New psychological diagnosis, n (%)  Anxiety disorder 25 (9)  Depressive disorder 15 (5)  Trauma or stress-related disorder 44 (15) New neurocognitive disorder diagnosis, n (%) 101 (35) Neurocognitive domain impairmentb, n (%)  Processing speed 78 (27)  Attention and executive functioning 155 (54)  Memory 89 (31)  Semantic fluency/confrontation naming 55 (19)  Visual spatialc 18 (17)  Fine motor 95 (33) Referred for follow-up neuropsychological assessment, n (%) 164 (57)

aAssessed differently by the two programs: the St. Louis program asked parents at the time of their appointment if they had concerns, and the Portland program abstracted these data from parent responses on Patient-Reported Outcomes Measure Information System reports.

bNeurocognitive domain impairment defined by individual assessment scores more than 1.5 sds below standardized population mean.

cAssessed only in St. Louis.

Psychological Screening

At the time of their PICU follow-up appointment, nearly half of patients or their parents/caregivers (48%) reported some type of patient emotional or behavioral concern (Table 3). Based on expert assessment, 29% of patients met criteria for a new psychological diagnosis, most commonly post-traumatic stress disorder or post-traumatic stress symptoms (15% of patients overall, 52% of all patients with a new psychological diagnosis). Depression was the least common diagnosis (5% of all patients, 17% of all patients with a psychological condition).

Neurocognitive Testing

Of the 289 patients that underwent neurocognitive screening testing in the follow-up clinics, over a third (35%) met criteria for a new neurocognitive diagnosis (Table 3). Neurocognitive domains regulated by the executive functioning system were the most commonly affected, including attention (54%), memory (31%), and processing speed (27%). Over 80% of patients in the programs were given new recommendations for school, for both new academic services and new classroom accommodations (Table 4). Many of these new accommodations were to support memory and executive function and to provide more time for completion of tests and tasks (Table 4). Most patients in both programs were referred for repeat or additional neuropsychological testing in the future (Table 3). All the children who live in Oregon and presented to the Portland program with a TBI were provided with a referral to the Oregon Department of Education’s Traumatic Brain Injury Liaison team.

TABLE 4. - New Recommendations Made for School From Neuropsychological Evaluations During the Acute Recovery Phase After PICU Discharge New Recommendations for Return to School, n (%) Total Population (n = 289) Service categories:  New IEPa 46 (16)  New 504 planb 57 (20)  Expand current IEP 49 (17)  Expand current 504 plan 17 (6)  Evaluate for services (i.e., suggestion for response to intervention) 33 (11) Accommodation categories:  New school-based occupational therapy treatment 21 (7)  New school-based physical therapy treatment 5 (2)  New school-based speech and language therapy treatment 9 (3)  Extended time on tests 169 (58)  Extended time on assignments 178 (62)  Preferential seating 56 (19)  Reduced test length 11 (4)  Separate setting for test taking 118 (41)  Reduced test assignment length 135 (47)  Reduced motor/handwriting demands 29 (10)  Access to assisted technology 40 (14)  Graduated return to school 28 (10)  Extra breaks 134 (46)  Extra access to water or other nutritional compounds 9 (3)  Extra access to nursing staff for things like prescribed medications 10 (3)  Vision supports 22 (8)  Auditory supports 51 (18)  Written copies of notes 37 (13)  Instructions read aloud 5 (2)  Other physical supports 19 (7)  Behavioral modification supports 11 (4)  Emotional adjustment supports 29 (10)  Executive functioning supports 92 (32)  Memory supports 58 (20)  Social supports 12 (4)  Exemptions from classes and activities such as physical education (even if only temporary) 10 (3)  Extra support for absences due to medical visits 23 (8)  Home-based strategies 43 (15)

IEP = individualized education plan.

aIEP, which focuses on direct services that can be provided by the school district to support a student’s learning process, such as physical therapy or speech therapy.

b504—refers to section 504 of the U.S. Rehabilitation Act of 1973, which states that any organization that receives federal funds cannot discriminate against children with disabilities. It provides assurance that all students have equitable access to an educational environment and is designed to remove barriers limiting a disabled child’s ability to receive an education. This includes allowing for extra time to complete tasks, use of textbooks in a format they can understand, such as audiobooks, etc.

St. Louis Program School Liaison Support

Between 2019 and 2021, the school liaison in St. Louis met with all 57 families who presented to clinic after her hiring, and 93% of those meetings resulted in some form of communication with the child’s school (email or phone call). Almost 85% of families (n = 48) received advocacy regarding school concerns, such as assistance with reintegration planning, or information regarding special education or homebound services, and 68% also received help providing their schools with requested documentation (i.e., discharge summaries, neuropsychological reports, and therapy reports). The school liaison attended individualized education plan or school planning meetings for more than a third of families (n = 21) in order to provide support and advocacy to parents.

DISCUSSION

One month after discharge from the hospital, more than a third of PICU survivors with acquired primary or secondary brain injury have identifiable neurocognitive impairments on a screening neuropsychological battery, particularly in executive function domains, consistent with prior studies that also found deficits related to executive functioning after critical illness in childhood (7,26). However, in contrast to other centers who report only 24% of PICU survivors receiving homebound services for school after hospital discharge, and only a third having conversations with their pediatrician about return to school (27), nearly every child in our programs have access to these services. Indeed, over 80% of our patients received intervention with specific recommendations for optimizing their return to school. Although a much higher proportion of patients in the St. Louis program received recommendations for new education plans compared with patients in Portland, the variance is likely in large part due to protocol differences; children seen in Portland are mostly given recommendations for new education accommodation plans in later clinic visits. However, even without formal education plans, support and accommodations are often recommended. There was more similarity between the two programs in the types of accommodations recommended, despite local context differences, highlighting similar assessment results.

Although our targeted neuropsychological evaluations do not directly assess academic skills, they do evaluate skills that underlie academic performance. For example, executive function difficulties can make it hard to start tasks, stay on task, plan ahead, organize, control impulses, and keep track of possessions. Executive function difficulties can also impact emotional/behavior regulation, resulting in behavioral outbursts, decreased frustration tolerance, and fast changes in mood. Processing speed difficulties can make it harder for a student to keep up with the pace of instruction and follow instructions. Immediate attention/working memory difficulties can make it harder for a child to complete a math problem, impair reading comprehension, and limit written expression; such difficulties also increase the risk for missing pertinent details and for falling behind in schoolwork. For many children, the presence or severity of these deficits after critical illness are not noticed or fully appreciated until after the child has returned to school and problems begin to arise. Indeed, as seen with our data, parents/caregivers more frequently notice the behavioral impacts of these challenges but may not appreciate the academic consequences in the home environment. Neuropsychological testing early in the process of return to school can alert a family and teachers to the areas where the returning student may be expected to have challenges.

School encompasses the primary physical, social, and intellectual engagement in most children’s lives, and the successful reintegration of a PICU survivor back into their academic environment is of paramount importance. However, in the first few months after returning home from the hospital, families are often still struggling with altered family and community relationships, and the PICU survivors themselves are only still in the early phases of their physical, emotional, and cognitive recovery. Recent work from other groups has highlighted the difficulties parents face when navigating their child’s school return alone and the clear potential for benefit when a recovering patient’s school attendance is systematically addressed (27). Given that our neurocognitive screening protocol requires only 30–45 minutes for administration and identifies the same concerns in the same proportions that longer testing batteries identify, we contend that early screening is feasible on a timely basis for families whose children are returning to school after a serious illness. When paired with our mental health and behavioral health surveys, our process also enables us to assist families with the psychological difficulties (e.g., anxiety/worry, hopelessness, frustration) that often accompany academic struggles as PICU survivors return to school (28). Given the widespread interest in expanding the small number of PICU follow-up programs available to survivors internationally (29), the most important message we may have to communicate is one of encouragement: a structured program using simple, publicly available screening tests and a short cognitive battery successfully identifies challenges likely to affect a child’s return to school, and immediately offers family support and solutions for those challenges.

It is possible that our study might be limited in its generalizability due to our teams’ longevity and dedicated interest in and experience with the PICU survivor population. We are comfortable with the testing process and interface with our local schools to a degree that few programs could match at their inception, and therefore our results may not be readily duplicated in other environments. We also recognize that relatively speaking, our teams are large and comprehensive and therefore require considerable resources to maintain service at the level we have described. While we have described a complete package of neurocognitive and psychological evaluation, not all components may be possible to administer in other settings. Both of our programs have grown and expanded over time, and neither started with the full consort of services described here. In our experience, any standardized approach to provide family support and screen for PICS symptoms will likely be well received by families and considered a rewarding and valuable experience by clinicians. However, we believe the testing protocol itself to be straightforward and have presented our process with a level of detail intended to permit newer programs to replicate our process in its entirety. Indeed, our goal is to share our approach as broadly as possible in order to promote greater unity in the structure and content of PICU neurocritical care follow-up programs nationally. We believe that this will yield the greatest amount of clinically comparable data and advance the field of PICU outcomes research more quickly than if follow-up programs develop in isolation. Last, we also acknowledge that our programs focus on the pediatric neurocritical care population, and as recent research demonstrates (30), there is clear evidence suggesting that the general PICU survivor population is likely at greater risk for adverse neurocognitive sequelae than we have previously understood. The extent to which our protocol would identify cognitive deficits in this larger patient population remains an area for future investigation.

CONCLUSIONS

Follow-up programs for PICU survivors should attend not only to physical and emotional aspects of recovery but also to the cognitive effects of critical illness. High prevalence of cognitive, behavioral, and psychological challenges underscores the importance of multidisciplinary assessment and intervention after discharge. The child’s successful reintegration back into school is an integral part of patients’ recoveries that can be facilitated with brief neurocognitive screening batteries.

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