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Abstract

Purpose

To explore convergent validity of the Physical and Neurological Examination of Subtle Signs Gaits and Stations completion scores (PANESS G/S) with Bruininks-Oseretsky Test of Motor Proficiency, Second Edition balance score – (BOT-2) and Activities-specific Balance Confidence Scale – (ABC) in typically developing youth with and without a history of concussion.

Method

Cross-sectional data obtained from 79 youth (32 with history of concussion) aged 10–17 years. First, between-group differences in balance measures were explored. Then, correlations were explored between demographic variables and balance measures to identify control variables for subsequent correlations between balance measures.

Results

Given no between-group differences on PANESS G/S, BOT-2, or ABC, correlations were examined across all participants. PANESS G/S was correlated with age. BOT-2 balance score was correlated with Full Scale Intelligence Quotient (FSIQ). Controlling for age and FSIQ, PANESS G/S was associated with better BOT-2 performance. PANESS G/S and ABC were not correlated.

Conclusion

This work adds to the literature characterizing the use of PANESS in adolescents, including those post-mTBI. Correlation between PANESS G/S and BOT-2 balance supports overlapping constructs. Lack of PANESS G/S correlation with ABC may reflect the lack of balance concerns in generally healthy youth and known discordance between performance and self-report measures.

Keywords

mild traumatic brain injury balance subtle sign adolescent

Introduction

Characterization of subtle motor skills is proving meaningful in children with mild traumatic brain injury (mTBI, concussion). The Physical and Neurological Examination for Subtle Signs (PANESS) is sensitive to change during clinical recovery from concussion,¹ distinguishes children who have clinically recovered from concussion from peers without a history of concussions,^1,2 and is associated with atypical functional brain connectivity in youth recovered from mTBI.^3,4 In addition, this test can be performed in adolescents in 15–20 min without specialized equipment, and^5,6 strong inter-rater reliability of scoring has been demonstrated.⁷

The PANESS consists of two main sections, Timed Motor (consisting of repetitive and sequential movements of both hands and feet and the tongue) and Gaits and Stations (G/S, consisting of gross motor/postural control tasks).⁷ Given the wide interest in postural control/balance as part of assessment for concussion, Saleem et al. evaluated which specific G/S items differentiated among children during recovery from concussion, after recovery from concussion, and those who have never had a TBI. Authors identified that both children recovering and recovered from mTBI performed worse on the hopping on one foot task than children who had never had a concussion⁸ The G/S completion scores (without accounting for overflow movements) have also been evaluated using Exploratory Factor Analysis based on data from 350 typically developing adolescents, revealing three factors: dynamic stability, movement strategies/ coordination, and underlying motor systems- musculoskeletal strength.⁹

Along with factor analysis, convergent validity contributes to construct validity for a measure, or the understanding of what is being assessed by the measure. Convergent validity has not been examined for the PANESS G/S completion scores.

Given that balance is commonly assessed as part of concussion evaluation, it would be useful to understand the relationship between performance on the PANESS G/S tasks and a standardized assessment of balance. Further, self-reported symptoms are a mainstay of concussion evaluation, though there is evidence that subtle motor assessments including the PANESS add sensitivity to detection of individuals with concussion.¹⁰ Thus, it would also be useful to understand the relationship between self-reported balance and PANESS G/S.

The primary goal of this study was to evaluate the relationship between performance on the PANESS G/S items (completion scores) and a) performance on the BOT-2 balance subtest and b) self-reported balance on the ABC, for the purpose of examining convergent validity of the PANESS G/S. Given lack of prior reports of use of the ABC in generally healthy youth, a secondary goal was to describe ABC scores from a healthy youth cohort.

Methods

All data were obtained from adolescents, aged 10–17 years at enrollment, as part of a larger, prospective, longitudinal study. One group of participants was enrolled after being medically cleared from a concussion/mild traumatic brain injury within 3 months from injury (history of concussion/mTBI). Medical clearance was defined as a clinician giving approval for a child to return to full participation in all high-risk sports/recreational activities without any modifications to the activity beyond typically recommended protective equipment. In addition, the caregiver and child endorsed full recovery from concussion. Exclusion criteria included a history of TBI with loss of consciousness for more than 30 min, post-traumatic amnesia > 24 h, evidence of intracranial findings on clinical imaging if completed, and mTBI without subjective return to baseline. Participants with history of concussion were eligible for 3 study visits: within 6 weeks of medical clearance and 3 and 12 months after the initial visit timeframe. Control participants were enrolled who had no history of suspected or confirmed traumatic brain injury including mTBI and were also eligible for three visits (initial and 3 and 12 months later). Potential participants with concerns/diagnoses of developmental/learning/mental health disorders or medical diagnoses or related treatments associated with potential for cognitive impacts (e.g., congenital heart disease, chronic prophylactic headache medication) were excluded from both groups.

As the study was ongoing before, during, and following the COVID-19 pandemic, some study visits were completed in-person, and some were completed virtually. Balance performance measures were only completed during in-person visits. For each participant, data included are from the study timepoint of the first administration of the performance-based measures (PANESS G/S and BOT-2) for that participant.

Ethical considerations

This study was approved by IRB; written informed consent was obtained from a parent or guardian, and assent was acquired from child participants.

Measures

Revised physical and neurological examination of subtle signs (PANESS)

The revised PANESS assesses subtle signs of motor impairment, including overflow and dysrhythmia during gait, balance, and timed activities in children.¹¹ PANESS is a standardized assessment that is sensitive to age-related changes^5,12 and has good test-retest,¹³ inter-rater reliability,⁷ and internal consistency.⁶ PANESS is designed to assess neurological subtle signs in children and adolescents and is most commonly used in individuals aged 5 to 17 years. Only the G/S items were used for this analysis specific to postural control/balance. G/S items involve the performance of various gait tasks including walking on heels, toes, and sides of feet; forward and backward tandem gait; maintaining stances of tandem stance with eyes closed, standing on both feet with eyes closed and with arms and fingers outstretched, and standing on one foot; and hopping. The Total G/S summary score reflects errors in performance as well as involuntary movements noted during task completion (e.g., tremor, overflow).⁵ Better performance is reflected by lower scores on the PANESS.⁶ To better reflect scoring of the other measures, only completion scores were used in analyses, representing performance without accounting for involuntary movements.⁹

Saleem et al.⁹ identified three latent factors from an exploratory factor analysis of G/S completion scores. These factors were named dynamic stability, movement strategies/ coordination, and underlying motor systems-musculoskeletal strength. The dynamic stability factor includes three walking tasks (walking on heels, walking on toes, and walking on sides of feet). The movement strategies factor is comprised of forward/backward tandem walking and standing feet together, eyes closed with arms and fingers outstretched. The last factor, underlying motor systems, includes tandem stance with eyes closed and standing and hopping on one foot.

Bruininks—oseretsky test of motor proficiency, second edition (BOT-2) balance subtest

The Bruininks—Oseretsky Test of Motor Proficiency, second edition (BOT-2) balance subtest is a standardized measure of balance with published norms for youth in this age range. Tasks assess trunk stability, stasis and movement, and visual cue usage.^14,15 The BOT-2 balance subtest has been frequently used for evaluating postural stability in research involving children with concussion^15–17 as well as more severe traumatic brain injury.¹⁸

Activities-specific Balance Confidence Scale (ABC)

The Activities-specific Balance Confidence Scale (ABC) was developed by Powell and Meyers

with the aim of evaluating confidence in balance among the elderly population at risk for falls.¹⁹ ABC is a self-report questionnaire with 16 items each querying confidence in balance in a different scenario. Scores reflect percent confidence in balance, with total scores ranging from 0 (no confidence) to 100 (complete confidence). The ABC illustrates excellent test-retest reliability, internal consistency, and validity.^20,21

To date, the ABC has primarily been studied in older adults. Hays et al.²² reported a positive correlation between the self-report measure, Activities-Specific Balance Confidence Scale (ABC) and clinical performance assessments including Community Balance and Mobility Scale (CB&M) and Balance Evaluation Systems Test (BESTest). A few studies have used the ABC as a balance assessment tool in non-elderly cohorts of patients with traumatic brain injury.^23,24 Inness et al.'s study found a correlation between the ABC and CB&M in adults receiving inpatient or outpatient neurorehabilitation after TBI.²⁴ The ABC has been used in children with overt motor impairment.²⁵ The strong psychometric properties of the ABC, in addition to prior use in individuals with TBI and children, contributed to the ABC being selected for use in the larger study.

Full scale intelligence quotient (FSIQ)

FSIQ was evaluated using the Wechsler Abbreviated Scaled of Intelligence, second edition (WASI-II) which consists of two subtests including Vocabulary (VC) and Matrix Reasoning (MR).²⁶

Statistical analysis

All analyses were performed with SPSS version 28. Statistical significance was considered p < 0.05. Normality was assessed by Shapiro-Wilk's test and data visualization. Outliers were identified by Z-score analysis with cutoff of ±3.29.²⁷

As a first step, independent T-test or Kruskal-Wallis tests (when there were significant threats to normality) and Cohen's d (for effect size) were used to confirm absence of systematic differences in balance measures between youth with and without history of concussion that could contribute to spurious associations between measures when examining across groups. Given little existing data on the ABC in children, ABC scores were further described (i.e., measures of central tendency) to meet the secondary objective of the study.

Prior to assessing agreement among measures, association of demographic variables with a) PANESS G/S, b) BOT-2 balance, and c) ABC were assessed using Pearson or Spearman correlations (for age and FSIQ) and T- or Mann-Whitney tests (for sex). Demographic variables found to be significantly associated with one or more balance measures were controlled for in subsequent analyses utilizing the associated balance measures. Correlations (Pearson's, Spearman's, or partial, depending on normality threats and whether there were associated demographic variables) were used to evaluate the association of PANESS G/S with BOT-2 balance and ABC. If significant correlations were identified, subsequent exploratory analysis of correlations of BOT-2 balance and/or ABC with the three PANESS G/S factors were completed. Strengths of correlation, r < 0.30, r = 0.30–0.50 and r > 0.50, were considered as weak, moderate, and strong correlations, respectively.²⁸ Convergent validity was defined as statistically significant, negative, correlation of moderate strength or higher²⁹ between PANESS G/S and BOT-2 balance or ABC (lower/better PANESS score associated with higher/better BOT-2 balance and/or ABC score).^27,30 Retrospective sample size analysis was performed to evaluate whether the sample size was sufficient to detect meaningful effects and to support the validity of the findings.

Results

Participant Characteristics

Seventy-nine participants were included in the study; 32 typically developing participants had a history of concussion and 47 did not. There were 41 male and 38 female adolescents, and overall median age was 13.8 years. For the youth with history of concussion, average time between mTBI and the first PANESS G/S measurement was 123.7 (SD = 113) days, and average time between medical clearance and first PANESS G/S measurement was 73 (SD = 95) days. PANESS and BOT data were normally distributed while ABC data were non-normally distributed. There was one outlier identified in ABC scores who did not appear to understand the written instructions for completing the

ABC correctly; that participant was excluded from analyses that involved the ABC. The median scores and IQR of PANESS G/S, BOT-2, and ABC are shown in Table 1. There were no statistically significant differences between the youth with and without a history of concussion with regards to sex, age, PANESS G/S, BOT-2 balance, or ABC (Table 1). Subsequent analyses were thus performed across the entire cohort of 79 youth.

Table 1.

Demographic and balance data by group.

Parameterseters	History of Concussion		No History of Concussion		Combined		between-group comparison
Parameterseters	% MED(IQR)	N	% MED(IQR)	N	% MED(IQR)	N	p	Effect size (Cohen's d)
Sex(male/female)	59/41	19/13	47/53	22/25	52/48	41/38	0.27
Age	13.6 (4.8)	32	13.8 (3.6)	47	13.8 (4.3)	79	0.27
PANESS Gaits and Stations	6 (6)	32	7 (5)	47	7 (6)	79	0.54	0.14
BOT-2 balance	34 (2.8)	32	33 (3)	47	33 (3)	79	0.67	0.10
ABC	96.3 (6.3)	32	93.1 (8.1)	46	94.7 (7.7)	78	0.10	0.14

MC post-mTBI, Medically Cleared post-mTBI; MED, Median; IQR, Interquatile range; N = number; PANESS, Physical and Neurological Examination of Subtle Signs; BOT-2 balance, Bruininks-Oseretsky Test of Motor Proficiency, Second Edition Balance subtest; ABC, Activities-specific Balance Confidence scale

ABC descriptives

The maximum reported total score of 100 was reported by 9 participants, and the lowest reported score was 67.5. Median ABC score was near the ceiling, at 94.7. Based on visual inspection of the distribution of scores (Figure 1), we further examined nine participants with ABC scores less than 80 (<80% confident across tasks). Scores in these 9 participants ranged from 67.50 to 79.38. Five of these participants did not have a history of concussion and four did. The most common activities for which low confidence in balance was reported were walking outside on icy sidewalks, walking in a crowded mall where people rapidly walk past you, and standing on a chair/standing on your tip toes to reach for something. These activities were also among those reported with lower confidence in chronic elderly stroke patients according to Botner et al.'s study, although the elderly stroke patients also report riding an escalator not holding the rail as an item among those with the lowest confidence.³⁰

Figure 1.

Plot of activities-specific balance confidence scale scores by age. Black dots represent control participants, and white dots represent participants MC post-mTBI. There was a weak correlation of ABC with age (r = .23, p = 0.04), with older participants reporting higher confidence. mTBI, mild Traumatic Brain Injury; ABC, Activities-specific Balance Confidence scale.

Association of demographic variables with balance measures

Age was moderately correlated with PANESS G/S (r = −.38, p = 0.001) and weakly correlated with ABC (r = .233, p = 0.04); in both cases, older age was associated with better scores. FSIQ was weakly positively correlated with BOT-2 balance score (r = .23, p = 0.04), with higher IQ associated with better balance performance.

Association of PANESS gaits and stations with BOT-2 balance and ABC

After controlling for age and FSIQ, PANESS G/S was significantly, moderately and negatively correlated with BOT-2 Balance (r = -.476, p < 0.001) (Table 2), with better PANESS performance associated with better BOT-2 performance (Figure 2). Effect size (f² = 29) contributed to high power (.996) for this correlation when retrospectively examined. In subsequent exploratory analyses, BOT-2 balance score was significantly negatively correlated with all three PANESS G/S factors with correlations of weak to moderate strength (Table 2).

Figure 2.

Relationship between PANESS gaits and stations and BOT-2 balance subtest. Partial correlation plot of PANESS G/S with BOT-2 balance subscale, controlling for age and FSIQ, demonstrating moderate correlation (r = -.48, p < 0.001). Better performance on PANESS G/S was associated with better BOT-2 balance performance. PANESS G/S, Physical and Neurological Examination of Subtle Signs Gaits and Stations; BOT-2 balance, Bruininks-Oseretsky Test of Motor Proficiency, Second Edition Balance score.

Table 2.

Partial correlations between PANESS gaits and stations and BOT-2 balance, accounting for age and FSIQ.

Control Variables	Variables	BOT-2 Balance
Control Variables	Variables	R	p-value
Age FSIQ	PANESS G/S	−.48	P < .001
	Factor 1 Dynamic Stability	−.40	P < .001
	Factor 2 Movement strategies/ Coordination tasks	−.28	P = .014
	Factor 3 Underlying motor systems	−.40	P < .001

PANESS G/S: Physical and Neurological Examination of Subtle Signs Gaits and Stations ; BOT-2 balance, Bruininks-Oseretsky Test of Motor Proficiency, Second Edition Balance score; FSIQ, Full Scale Intelligence Quotient.

There was no significant correlation between PANESS G/S and ABC (r = .03, p = 0.81) (Figure 3). Low effect size (f² = .0009) for this correlation supports a lack of overlapping constructs between these two measures.

Figure 3.

Relationship between PANESS gaits and stations and activity-specific balance confidence scale. Partial correlation plot of PANESS G/S with ABC, controlling for age, demonstrating no significant correlation between PANESS G/S and ABC (r = .03, p = 0.81). PANESS G/S, Physical and Neurological Examination of Subtle Signs Gaits and Stations; ABC, Activity-specific Balance Confidence scale.

Discussion

Our primary goal was to evaluate agreement among PANESS G/S completion scores and other balance assessments included in this larger study of typically developing youth with and without a history of concussion, specifically the BOT-2 balance subtest and self-reported ABC. After controlling for related demographic variables, correlations support convergent validity of PANESS G/S with BOT-2 balance subtest.

Convergence between PANESS G/S and BOT-2 was expected in light of the two performance measures consisting of similar and overlapping tasks. Both measures were designed to evaluate balance in children, with the PANESS additionally capturing broader aspects of postural control.

Exploratory analyses demonstrated convergent validity (based on correlations of at least moderate strength) with two of the three previously identified PANESS G/S factors⁹ Dynamic Stability (Factor 1) and Underlying Motor Systems (Factor 3).

PANESS G/S Dynamic Stability (Factor 1)⁹ involves three walking tasks, all in the forward direction, and the walking tasks on the BOT-2 are also all in the forward direction. Similarly, PANESS G/S Underlying Motor Systems (Factor 3) is comprised of a combination of standing/hopping on one foot and tandem stance with eyes closed, which also overlap with testing positions in the BOT-2 balance subtest. On the other hand, PANESS G/S Movement Strategies/Coordination tasks (Factor 2) includes backwards tandem gait and a feet together stance with eyes closed, arms and fingers outstretched, tasks associated with greater perturbations and larger postural sway than other tasks performed with eyes open and a wider base of support.⁹ The BOT-2 balance subtest does not include similar items, which likely explains the lowest correlation and lack of convergence for this PANESS G/S factor when examined independently.

The overall cohort scores near the ceiling of the ABC highlights the difference in the intent of the development of this measure (to capture variability among elderly) with that of the PANESS and BOT-2 (to reflect subtle and developmental changes in motor function in children and adolescents). The lack of correlation between measures reinforces this divergence in sensitivity to the studied population. Furthermore, lack of agreement between self-report and performance-based measures.^31,32

Our second goal was to describe ABC scores in a healthy youth cohort. As would be expected, this cohort self-reported high levels of confidence in their balance overall (median score 94%) on this questionnaire originally designed for use in elderly population. This cohort scored higher than a prior cohort of United States military service members (mean age 34 years) evaluated through an intensive outpatient program for concern for persisting post-concussive symptoms, for which mean score was 81%.³³ While concussion and vestibular function can disturb confidence in balance, the children with a history of concussion included in our cohort had been medically determined to be recovered from concussion and reported resolution of any concussion symptoms, consistent with their overall high confidence in balance. It is noted that some more challenging scenarios queried on the ABC did elicit more variability in confidence from even this healthy/recovered cohort of youth, and it is unknown whether or not the ABC scores would have been lower if youth were studied while still symptomatic from concussion. The overall high level of self-confidence in balance is consistent with the lack of differences observed between the youth with and without concussion on the performance-based balance measures. While prior studies^1,2 have reported that youth with a history of concussion perform worse on PANESS Gaits and Stations than typically developing youth without a history of concussion, those studies differed in that they evaluated the Summary/Total Gaits and Stations Score rather than the G/S completion scores, as used here. This highlights the potential importance of including more subtle features of motor task performance (e.g., motor overflow) when characterizing performance in individuals who have recovered from mTBI.⁷

This evaluation of convergent validity of the PANESS G/S was limited by measures included in the larger study through which these data were collected. The Balance Error Scoring System (BESS),³⁴ a National Institute of Neurological Disorders and Stroke (NINDS) Sport-Related Concussion core common data element,³⁵ was not included in the study due to use in an affiliated concussion specialty clinic which could bias findings due to prior exposure in the youth with a history of concussion but not those without a history of concussion. Another limitation is the relatively small sample size for examining psychometric properties of a measure, though examination of effect size/retrospective power analyses supported the findings with the available sample size. While this study was not designed to do so, future studies with larger sample sizes could examine, via regression analyses, whether history of concussion or any other factors moderate the relationships among the balance measures, and use of a regression approach could also eliminate bias from multi-step procedures.

Conclusion

This study contributes to the construct validity of the PANESS Gaits and Stations items through demonstration of significant correlation with a validated, age-appropriate performance-based measure of balance. In addition, this work adds to the description of the Activities-specific Balance Confidence Scale through examination in a generally healthy cohort of youth. Overall, this work suggests that continued characterization of subtle motor function through tools including the PANESS may provide insights for evaluation and optimization of recovery after youth concussion.

Footnotes

Acknowledgements

We confirm that this research is original and has not been published elsewhere. We declare no conflict of interest regarding the publication of this research. The authors have no acknowledgments.

Funding

The authors disclosed receipt of the following financial support forthe research, authorship, and/or publication of this article: This study was supported by the National Institutes of Health (S.S.: R01HD090266).

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

ORCID iD

Sopatip Rerkmoung

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Convergent validity of physical and neurological examination of subtle signs (PANESS) gaits and stations with performance-based and self-reported balance measures

Abstract

Purpose

Method

Results

Conclusion

Keywords

Introduction

Methods

Ethical considerations

Measures

Revised physical and neurological examination of subtle signs (PANESS)

Bruininks—oseretsky test of motor proficiency, second edition (BOT-2) balance subtest

Activities-specific Balance Confidence Scale (ABC)

Full scale intelligence quotient (FSIQ)

Statistical analysis

Results

Participant Characteristics

ABC descriptives

Association of demographic variables with balance measures

Association of PANESS gaits and stations with BOT-2 balance and ABC

Discussion

Conclusion

Footnotes

Acknowledgements

Funding

Declaration of conflicting interests

ORCID iD

References