Bryce Yale, SPT1, Laura Greiss Hess, PhD, OTR/L2, Micah Mar, SPT1, Alejandra Roque, PT, DPT3, Dana Jacobs, PT,1, Janice Brown, OTS2, Jordan Ng2, OTS, Reilly Todd2, OTS, Alyssa Vo, OTS2, *Kathryn C. Nesbit, PT, DPT, DSc2
- University of California San Francisco/San Francisco State University Graduate Program in Physical Therapy
1600 Holloway Ave. San Francisco CA 94132
- Dominican University of California, Department of Occupational Therapy
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- NAPA Center Inc.
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* Corresponding Author
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Pediatric stroke has a significant impact on children and families. Outcome measures are essential to guide clinical management and inform research priorities, yet these instruments are highly varied in scope and application. Because pediatric stroke care and research is evolving, there is a need for a current review of pediatric stroke outcome measures. The purpose of this study was to systematically review the current literature for pediatric outcome measures, describe the studies using pediatric outcome measures, and describe the outcome measure characteristics.
From an initial search of 1625 articles with duplicates removed, 116 articles met inclusion criteria. In those 116 articles, 95 distinct outcome measures were identified. Our review noted the most used outcome measures focused on deficits of the child whereas there was a paucity of outcomes used that included patient and family perspectives, recovery in natural contexts (e.g., home, school, community), and inadequate representation executive function and quality of life. We also found a lack of reliable and valid outcomes for the pediatric hemorrhagic stroke population, and a limited amount of outcomes that measure recovery over time.
The findings in this systematic review support recommendations for future development and use of pediatric stroke outcome measures, particularly for pediatric hemorrhagic stroke, that better capture the impacts to child and family life and contextually meaningful aspects of recovery over time.
Pediatric stroke, despite its reduced incidence when compared to many other childhood conditions, is a major cause of lifelong neurological disability and remains one of the top ten causes of death in childhood.1,2 The pediatric ischemic stroke incidence rate is 2.7 per 100,000 and the hemorrhagic incident rate is 1.7 per 100,000.3 While the incidence of hemorrhagic stroke is less than ischemic stroke, death rate, and morbidity as measured by Disability-Adjusted Life Years (DALYs) were reported to be 6-7 times higher.4 Despite advances in the treatment of both ischemic and hemorrhagic stroke, 1 of 10 children with pediatric stroke have a recurrence within 5 years.2
Recovery from pediatric stroke is assessed by outcome measures that vary in their scope, timing, use, and domain. Based on the International Classification of Functioning, Disability and Health (ICF) model,5 outcome measures may assess difficulties with body structure and function (impairments), difficulties executing tasks (activity limitations) and difficulties with carrying out life roles in the home, school, or community (participation restrictions). Some outcome measures are patient-centered, including patient perspectives, preferences, and values.6 Others are family-centered, affording the family the opportunity to self-report and/or collaborate with the person administering the assessment.7 Outcome measures can be psychometrically reliable and valid for specific purposes: discriminative (a measurement at a one point in time), evaluative (repeated to show progress over time), or predictive (associated with a future condition).8 Outcome measures are often shown to be reliable and/or valid for specific populations. Timing of outcome measures can vary from administration early in recovery to long-term assessment. Malone and Felling9 noted that the variability of outcome measure type and timing in pediatric stroke recovery contributes to the difficulty making comparisons across studies.
A robust battery and a clear understanding of the application of outcome measures essential for clinical care and ongoing research. Current literature notes the need for outcome measures to capture the nuances of pediatric stroke recovery based on injury to the developing brain, rather than reliance on assumptions based on adult stroke.9,10 Additionally, current literature noted the importance of patient- and family-centered outcomes in providing meaningful, contextually relevant perspectives on long-term implications of disability from pediatric stroke.11,12 In 2012, Englemann and Jordan completed a systematic review of outcome measures utilized in pediatric stroke studies and identified 36 studies using standardized measures, with 38 unique outcome measures noted.10 Importantly, Porcari, et al13 noted that the lack of pediatric stroke specific outcome measures made it difficult to determine the effectiveness of immediate and long-term interventions.
Pediatric stroke has a significant impact on children and families while outcome measures guide clinical management, rehabilitation and inform research priorities. Because pediatric stroke care and research is evolving, there is a need for a current review of pediatric stroke outcome measures for scope, application, and timing. It is essential to examine the characteristics of the outcome measures, including those that capture the perspectives and experiences in real-life contexts of the children and families.
The purpose of this study was to systematically review the current literature for pediatric outcome measures, describe the studies using pediatric outcome measures, and describe the outcome measures characteristics. A clear understanding of the has important implications for the direction of current efforts to develop pediatric stroke registries14 and research protocols, especially for the less-studied pediatric hemorrhagic stroke population. The specific aims of this study were to examine the literature for (1) type of study and level of evidence, (2) timing of outcome measure administration post-stroke, (3) number of outcome measures used in each study (4) and the number of times an outcome measure was used across studies. Further aims included analyses of the outcomes measures found in the literature themselves and included: (1) ICF levels (body structure and function, activity, participation), (2) domains (motor, cognitive, quality of life, social-emotional, executive function), (3) contexts (home, school, community), (4) perspectives of patient and family, (5) type (discriminative, evaluative, predictive), and (6) reliability and validity for pediatric stroke.
This systematic review had the following inclusion criteria: prognostic or intervention study articles from 2000-2021, population n > 3, population age > 28 days through 18 years, population diagnosis of ischemic and/or hemorrhagic stroke, study included named functional outcome measures, and article is full text in a peer-reviewed journal. Studies were excluded if they were diagnostic or cost-effectiveness studies as well as if the study population was perinatal, neonatal, adult, or post-trauma. This systematic review was determined to be exempt by the institutional review board.
Search terms included: pediatric stroke, pediatric ischemic stroke, pediatric hemorrhagic stroke, pediatric stroke outcome measures (including alternate spelling of all terms).
Initial electronic searches of PubMed, Cumulative Index to Nursing and Allied Health Literature (CINAHL), Elton B. Stephens Company (EBSCO), Google Scholar, and Cochrane Library were performed in September 2021 with the final search on June 15, 2022.
After duplicates were removed from the initial search list, records were screened by title and abstract by two authors and excluded by relevance. Remaining records were sought for retrieval, and full text articles were assessed by two authors for eligibility based on the inclusion criteria. If there were any discrepancies related to eligibility criteria, a third author was included to reach a consensus. The study type and strength of evidence was reviewed by two authors.
Figure 1 is the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) flow diagram.15 Outcome measures named in the studies were then identified. Each outcome was reviewed by two authors. If there were any discrepancies related to the outcome characteristics, a third author was included to reach a consensus. The outcome measure characteristics were determined through a variety of resources such as the outcome measure website, available outcome measure protocols, outcome measure databases, and information in the included article itself. Descriptive statistics (frequencies) were used to examine the article and outcome measure characteristics. Post-analysis weighting based on the frequency of the use of the outcome measure in the study articles was used to report on the weighted outcome measure characteristics.
Articles, levels of evidence, and time of study
The initial search returned 1625 articles once duplicates were removed. After assessment for inclusion criteria, 116 articles were included in the review13, 16-130 Reasons for exclusion included inability to access articles, study type, lack of outcome measures, study population characteristics, and number of study participants (PRISMA flow diagram, Figure 1).15 From the 116 articles detailed in Appendix 1, 95 unique outcome measures were identified. Appendix 2 is the PRISMA checklist.15
Of the 116 included studies, 91 were prognostic studies looking at factors which influence outcomes in the pediatric stroke population (78.5%). Most of these were Level 2B retrospective cohort studies (59.3%), and less than half (40.7%) were prognostic case series or cross-sectional studies (Level 4).131 Only 21.6% (n=25) were intervention studies looking at the effectiveness of treatment interventions in the pediatric stroke population. More than half of the intervention studies were Level 4 case-series or cross-sectional studies (61.9%). 131 Other intervention studies (52.4%) were Level 2B individual longitudinal cohort studies with a control group and one Level 1B randomized control trial (4.8%).131 Overall, most prognostic and intervention studies were Level 2B with only one higher level (1B) study, and many studies were Level 4.131 Of the 116 articles, 91.4% of the studies were set in Upper-Income Countries, 6.0% were set in Upper-Middle Income Countries, and 5.2% were set in Lower- and Middle-Income Countries. Four studies included centers in countries with two different income levels. Appendix 1 contains details of the levels of evidence and countries represented by each study.
Time the outcome measures were administered relative to the stroke
Our analysis revealed a wide range of outcome measure administration timing relative to the time of the stroke. Outcome measure administration timing ranged from time of injury to 11.5 years post-stroke. The mean was 2.4 years post-stroke (SD=2.9) (median and mode = 1-year post-stroke). Frequency of outcome administration timing was most often once, with a range of one to five times, and an average of 1.2 times (SD=0.8). In general, outcomes were measured post-acutely, most at one year, and at one time during recovery. Figure 2 is a summary of the age ranges and percentage of outcomes administered at that age (using n=133 outcomes noted in the articles with some studies administering outcomes more than once and some studies not clearly indicating the timing).
School function measured in the studies
Approximately a third (31.0%) of the 116 studies included a measure related to school. The school measure characteristics included a range of factors including school function or questions about school attendance, grades, type of school, or type of support at school (31.0%, n=36). In the 36 articles that included school function, 25 of them (69.4%) used an outcome measure, while 11 used less standardized questionnaires or surveys.
Number of outcomes used in each study
Within the 116 articles, our results showed a range of the number of outcome measures used from 1 to 15 unique measures. The mean number of outcome measures used was 3.0 (SD = 2.7) (median = 2, mode = 1).
Frequency of outcome use across studies
The most frequently used outcome measures were the Pediatric Stroke Outcome Measure (PSOM) (50 times) and the Modified Rankin Scale (mRS) (45 times). Both the PSOM and the mRS were used 48.0% more than the next most frequently used outcome measure, the Pediatric National Institutes of Health Stroke Severity Scale (PedNIHSS) (27 times). On average, each outcome measure was used 3.8 times (median = 2, mode = 1). Of the 95 outcome measures, only 33 were used more than twice, and only 7 were used more than 10 times.
Table 1 includes names and characteristics of the top 10 most frequently used outcome measures.
International Classification of Functioning, Disability, and Health (ICF) levels of all outcome measures
Our analyses of outcome measure characteristics included an examination of ICF levels. ICF activity level was more frequently when compared to body structure and function and participation (61.1%, 46.3%, and 45.3% unweighted respectively). When weighting the outcome measures based on their frequency of use, activity level measures were used about three quarters of the time (78.0% weighted), body structure and function measures a little over half the time (60.0% weighted) and participation level measures about a quarter of the time (28.9% weighted). Figure 3 includes the comparison between the weighted and unweighted frequencies of these ICF level characteristics for all outcome measures. Appendix 3 is a table of the details of the ICF levels of all outcome measures.
Domains of all outcome measures
Our analyses of outcome measure characteristics included an examination of domains – cognitive, motor, and social domains were most frequently measured (48.4%, 44.2%, and 28.4% unweighted respectively). The least frequently measured domains were executive function and quality of life (5.3% and 15.8% unweighted respectively). When weighted based on frequency of use, cognitive, motor, and language domains were most frequently measured (74.1%, 63.4%, and 49.9% weighted respectively). With weighting also, the least frequently measured domains were executive function and quality of life (5.5% and 27.6% weighted respectively). Figure 3 includes the comparison between the weighted and unweighted frequencies of these domain characteristics for all outcome measures. Appendix 3 is a table of the details of the domains of all outcome measures.
Context of all outcome measures
We then analyzed the contexts of the outcome measures. About a third of the outcomes measured home function (30.5% unweighted), about a quarter of the outcomes measured school function (24.2% unweighted), and about a third of the outcomes measured community function (35.8% unweighted). Note, some measures included both home and community function. When weighting the outcome measures based on their frequency of use, less than a quarter of the outcomes measured home (18.7% weighted), school (16.5% weighted) and community (23.1% weighted) function. Figure 3 includes the comparison between the weighted and unweighted frequencies of these context characteristics for all outcome measures. Appendix 3 is a table of the context details of all outcome measures.
Patient and Family Perspectives of all outcome measures
We analyzed whether the patient or family perspectives were included in the outcome measure through a patient or family survey element (e.g., experience, preferences, rankings, goals, etc.), Approximately a quarter of the outcome measures include direct input from the patient perspective (27.4% unweighted). However, when weighted based on frequency of the use of the outcome measures, outcome measures included direct input from the patient perspective less than a quarter of the time (14.3% weighted). Direct input from family perspectives were included in slightly less than a quarter of the outcome measures (22.1% unweighted). This percentage stayed close to the same when weighted based on the frequency of the use of the outcome measures (20.7% weighted). Figure 3 includes the comparison between the weighted and unweighted frequencies of these perspective characteristics for all outcome measures. Appendix 3 is a table of the details of the perspectives of all outcome measures.
Type of all outcome measures
When the type of outcome measure was considered, all outcome measures (n=95) were discriminative (100.0%) providing an assessment of the current functioning at a single point in time. Approximately a quarter (25.3%) of the measures were evaluative, and a smaller percentage were predictive (14.7%). With weighting based on frequency of use, approximately a quarter of the measures were evaluative (27.8%); however, over a third were predictive (35.5%).
Reliability and validity for pediatric stroke across all outcome measures
Only 6 outcome measures had some reliability and validity for the pediatric ischemic stroke population. No outcome measures had reliability and validity specifically for the pediatric hemorrhagic stroke population. With weighting based on frequency of outcome use, a measure with reliability and validity for pediatric ischemic stroke was used approximately a quarter of the time (24.5%). In contrast, a measure with reliability and validity for pediatric hemorrhagic stroke was used 0.0% of the time.
Most frequently used outcome measures summary
Table 1 is a summary of the 16 most frequently used outcome measures in the 116 study articles (outcomes that were used 5 or more times) and their characteristics weighted based on their frequency. Appendix 4 includes details about these outcome measures. Figure 4 includes the comparison between the weighted and unweighted frequencies of the characteristics for the 16 most frequently used outcome measures. In summary, activity ICF level was included most frequently in the outcome measures, and participation ICF level least frequently. Motor and cognitive domains were most frequently represented while executive function and quality of life were least frequently represented. The contexts of home, school, and community were infrequently included with school function being the context included least frequently. Patient and family perspectives were also included infrequently in these 16 most frequently used outcome measures. The age range for the 16 most frequently used outcome measures was 0-90 years, with the most common age range of 2-17 or 18 years. For several outcome measures, the condition (ischemic stroke) was specified rather than a specific age.
The results of this systematic review revealed important information about the use of pediatric stroke outcome measures by describing the frequency, application and characteristics of the outcome measures used. Outcome measures inform the clinical management and research of pediatric stroke care; therefore, how often they are employed, what they measure, and how they measure it have implications for the recovery journeys of children and families. In summary (Figure 5):
- Ninety-five distinct outcome measures were identified.
- All outcomes were discriminative, some were evaluative, and few were predictive.
- Few outcome measures had some reliability and validity for pediatric ischemic stroke, but none had reliability and validity for pediatric hemorrhagic stroke.
- Most outcomes were administered post-acutely at one year, and at one point in time.
- Most studies used one outcome measure; however, there was a wide range in the number of outcome measures used.
- On average, each outcome measure was used 3-4 times across the 116 studies; however, most were used only once, and only a few were used more than 10 times.
- From the perspective of ICF levels, the activity level was most represented in the outcome measures, and the participation level the least represented.
- Motor, cognitive, social and language domains were most frequently measured and executive function and quality of life were least frequently measured.
- Few outcome measures related to home, community, or school function.
- Few outcome measures included perspectives from the patient or family.
- When the characteristics of the outcome measures were weighted based on the frequency of use within the study articles, the paucity of participation level, real-life contexts (home, school, community), and both patient- and family-centered characteristics was noteworthy.
Our results revealed an increase in the number of studies using pediatric stroke outcome measures as well as the number of distinct outcome measures used when compared to previous literature.10 For example, in 2012, Engleman and Jordan10 identified only 36 studies and 38 unique outcome measures compared to our finding of 116 included articles and 95 outcome measures. These trends suggest an increased awareness of the need for specific pediatric stroke outcomes. The Pediatric Stroke Outcome Measure (PSOM) was the most frequently used outcome measure identified in our study and this outcome was very new at the time of the Engelman and Jordan review.10 However, because the PSOM and many of the top 10 most frequently used outcomes do not include home, school, or community function, and do not include patient and family perspectives, meaningful information from outcome measures about the real-life experiences during stroke recovery is lacking.
This systematic review revealed that pediatric stroke outcomes less often include contextual and functional areas. Specifically, deficiencies in outcome measures for pediatric stroke were the limited opportunity for inclusion of patient and family perspectives, the infrequent consideration of recovery in a real-life context (home, school, community), and inadequate representation and inclusion of all domains important to stroke recovery (executive function, quality of life). We also found a lack of reliable and valid outcomes for the pediatric hemorrhagic stroke population, and limited amount of longitudinal outcome measurement. These gaps illuminate a skewing of outcome measurement data being more deficit focused and not broadly inclusive of child and family centered care within meaningful, daily contexts. Therefore, the underutilized types of outcome measures are critically important.
The first area of shortcoming is including patient and family perspective in the outcome. Our efforts to provide patient- and family-centered care are hindered by a lack of use of measures that include patient and family perspectives and on outcomes that focus on the experiences of children and their families as they return to life at home, school, and in the community. Mangin, et al.6 noted that the scarcity of tools for identifying patient priorities was a barrier to shared decision making. We found that despite the premise that promoting patient-centered care can optimize health outcomes, few outcome measures encourage patient collaboration. Clay and Parsh7 noted that “a patient’s health care decisions should be contextualized in terms of a patient’s broader life experiences” including the role of family members (p.40). McKevitt, et al.132 reported a variety of parent experiences based on the child’s needs and family situation, with a theme in their work being the impact of the child’s stroke on the parent as well as the family’s well-being. Unfortunately, as our results indicate, the family perspectives are often overlooked and not commonly included in chosen outcome measures.
The second area of shortcoming is in gathering information about recovery in a real-life context. The current literature highlighted the importance of understanding the needs of children post-stroke as they return to school. Hawks, et al.169 described educational placement of following hemorrhagic stroke and noted that although almost all children were able to attend school post-stroke, most children required educational modifications. Gordon, et al.10 reported that over two thirds of families and children reported unmet needs post- stroke; over half reported difficulties in school-related activities and over one third had difficulties in leisure activities and social relationships. The American Heart Association/American Stroke Association Scientific Statement on stroke management in neonates and children noted school-based needs in this population.134 Again, unfortunately, our results revealed limited consideration of real-life contexts employed in the frequently used outcome measures.
The third area of shortcoming is in capturing domains important to stroke recovery. The literature suggests the importance of executive function and quality of life for children with disabilities.135,136 and these domains were infrequently measured by current outcome measures. The fourth area of shortcoming is the lack of reliable and valid outcome measures for hemorrhagic stroke in the pediatric stroke population – a population with a high mortality and morbidity burden. Lastly, the fifth area of shortcoming is the lack of outcome measures used for longitudinal studies. Given the uncertain trajectory of pediatric stroke recovery on the developing brain as noted by Porcari, et al.13 and Malone and Felling,9 it is important for outcome measures to inform care management over time, not only with a focus on the immediate post-acute phase of recovery. Golomb and Lo,137 in their comment on the longitudinal study by Goegel Simonetti, et al.,60 noted that “Parents want to know if their children will be able to finish high school, attend university, hold a job, live independently and start families of their own.” (p.1917). We found most outcome measures are used to examine the patient’s condition at a single point in time (discriminative measures), only some were used to monitor progress over time (evaluative), and even fewer were designed to predict how a patient’s current function might indicate a level of disability or condition in the future (predictive).
Information about the outcome measures used in the studies in this systematic review was limited to what was available on outcome measure websites, available outcome measure protocols, outcome measure databases, and information in the included study article itself. We did not complete an extensive literature review and critique of each outcome measure beyond our inclusion / exclusion criteria. In addition, several studies used only parts of each outcome measure adding another limitation to this study’s interpretation. Although articles and outcome measures were reviewed by at least two authors, and if needed, a third author was used to resolve any discrepancies, the results may be influenced by a small group of reviewers. Outcomes in these studies represented those used in a research context and may differ from outcomes used in a clinical context.
Of note, we have examined quantitative measurement of recovery in real-life contexts and of patient and family perspectives. However, in clinical practice and qualitative research methodologies, information about real-life, as well as personal accounts of lived experiences from patients and families are often gathered through interviews and / or added to comment sections of outcome measures. Therefore, there are opportunities to expand current research to include more examination of qualitative data.
Implications and directions for future research
The findings in this systematic review support recommendations for future development and use of outcome measures for pediatric stroke, particularly for pediatric hemorrhagic stroke, that better capture meaningful aspects of recovery over time. Outcome measures with reliability and validity specifically for the pediatric hemorrhagic stroke population are needed. Development and use of outcome measures that include contextual elements of the patient’s recovery such as the home, school, and community as well as domains of executive function and quality of life are important. In addition, outcome measures that include patient and family perspectives would promote shared decision making, collaboration, and engagement in care. Clinicians and researchers would additionally benefit from resources to guide choosing and utilizing outcome measures beyond the medical model.
This study highlights the increasing use of outcome measures in a growing body of pediatric stroke research. With advancements in collaborative, interdisciplinary team pediatric stroke management and research, outcome measures are critical for guiding care and afford an opportunity to engage children and families in shared decision making. The lack of reliable and valid measures for pediatric hemorrhagic stroke is striking and will hopefully, in the future, follow the recent progress in development of outcome measures for pediatric ischemic stroke. Relevance of the outcomes used in pediatric stroke management to real-life contexts and consideration of patient and family perspectives are paramount to making health measures meaningful to children and their families.
The authors would like to acknowledge the multidisciplinary team at the University of California’s American Heart Association Bugher Center of Excellence in Pediatric Hemorrhagic Stroke.
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Tables + Appendixes
Outcome Measures in Pediatric Stroke: A Systematic Review