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\begin{document}

\title{A Prospective Study of Social Competence in Survivors of Pediatric Brain
Tumors}



\author[1]{May Albee}%
\author[2]{Santiago Allende}%
\author[2]{Victoria Cosgrove}%
\author[1]{Matthew Hocking}%
\affil[1]{The Children's Hospital of Philadelphia}%
\affil[2]{Stanford University School of Medicine}%


\vspace{-1em}



  
  \date{May 30, 2024}


\begingroup
\let\center\flushleft
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\endgroup





\selectlanguage{english}
\begin{abstract}
BACKGROUND/OBJECTIVES: Survivors of pediatric brain tumors (BT) are at
increased risk for difficulties with social competence, including poor
social information processing (SIP) and peer relationships. Due to
improved survival rates among BT, there is a need to better understand
these challenges and if they are specific to BT versus other survivors
of childhood cancer. METHODS: 51 BT and 34 survivors of pediatric solid
tumors (ST) completed evaluations of SIP and peer relationship quality
within 6 months of completing treatment and at one year follow-up.
Caregivers also completed a measure of social skills. Linear mixed
models evaluated (1) differences between BT and ST on SIP and social
skills and (2) how indices of SIP were associated with peer
relationships over time for ST and BT. RESULTS: BT did not differ from
ST on indices of SIP or social skills over time. There was a three-way
interaction between measures of SIP, group, and time to predict peer
relationships. ST showed a positive association between baseline social
skills and theory of mind and peer relationships over time, whereas BT
showed an inverse association between baseline social skills and theory
of mind and peer relationships over time. CONCLUSION: Baseline SIP and
social skills affected the trajectory of BT peer relationships. BT
social functioning should be monitored regularly after the completion of
treatment to determine if and when intervention services would be
beneficial.%
\end{abstract}%



\sloppy


A Prospective Study of Social Competence in Survivors of Pediatric Brain
and Solid Tumors

May Albee BS\textsuperscript{1}, Santiago Allende
PsyD\textsuperscript{2}, Victoria Cosgrove PhD\textsuperscript{2}, \&
Matthew C. Hocking PhD\textsuperscript{1,3}

\textsuperscript{1}The Children's Hospital of Philadelphia,
Philadelphia, PA

\textsuperscript{2}Stanford University School of Medicine, Palo Alto, CA

\textsuperscript{3}Perelman School of Medicine at the University of
Pennsylvania, Philadelphia, PA

Corresponding Author:

Matthew C. Hocking

The Leonard \& Madalyn Abramson Research Center

3615 Civic Center Blvd, Office 1427B

Philadelphia PA 19104

(267) 426-5561

hockingm@chop.edu

Abstract Word Count: 228

Manuscript Word Count: 3,106

4 Tables, 2 Figures

Key Words: Brain Tumor, Solid Tumor, Social Information Processing

Running Title: Social Competence in Survivors of Pediatric Cancer

Abbreviation Key\selectlanguage{english}
\begin{longtable}[]{@{}ll@{}}
\toprule
BT & Survivors of Pediatric Brain Tumors\tabularnewline
\midrule
\endhead
CNS & Central Nervous System\tabularnewline
ST & Survivors of non-CNS Solid Tumors\tabularnewline
SIP & Social Information Processing\tabularnewline
ASD & Autism Spectrum Disorder\tabularnewline
DANVA-2 & Diagnostic Analysis of Nonverbal Accuracy Child Faces
2\tabularnewline
SSiS & Social Skills Improvement System\tabularnewline
PROMIS & Patient Reported Outcomes Measurement Information
System\tabularnewline
PNORTI & Pediatric Neuro Oncology Rating of Treatment
Intensity\tabularnewline
NPS & Neurological Predictors Scale\tabularnewline
\bottomrule
\end{longtable}

ABSTRACT

BACKGROUND/OBJECTIVES: Survivors of pediatric brain tumors (BT) are at
increased risk for difficulties with social competence, including poor
social information processing (SIP) and peer relationships. Due to
improved survival rates among BT, there is a need to better understand
these challenges and if they are specific to BT versus other survivors
of childhood cancer.

METHODS: 51 BT and 34 survivors of pediatric solid tumors (ST) completed
evaluations of SIP and peer relationship quality within 6 months of
completing treatment and at one year follow-up. Caregivers also
completed a measure of social skills. Linear mixed models evaluated (1)
differences between BT and ST on SIP and social skills and (2) how
indices of SIP were associated with peer relationships over time for ST
and BT.

RESULTS: BT did not differ from ST on indices of SIP or social skills
over time. There was a three-way interaction between measures of SIP,
group, and time to predict peer relationships. ST showed a positive
association between baseline social skills and theory of mind and peer
relationships over time, whereas BT showed an inverse association
between baseline social skills and theory of mind and peer relationships
over time.

CONCLUSION: Baseline SIP and social skills affected the trajectory of BT
peer relationships. BT social functioning should be monitored regularly
after the completion of treatment to determine if and when intervention
services would be beneficial.

INTRODUCTION:

Survivors of pediatric brain tumors (BT) are increasing in number due to
advances in treatment over the past 20 years {[}1{]}. The original focus
on survival for this population has shifted over time to encompass the
cognitive, physical, and social ramifications of disease and treatments
on individuals from diagnosis through the course of their lives. With a
more holistic understanding of the impact of cancer treatment on the
developing central nervous system (CNS), more recent research has shown
that BT are less likely than typically developing peers to go to
college, live independently, have close friends, and marry {[}2{]}. In
the short-term, BT also struggle socially and are less likely to
establish friendships compared to survivors of non-CNS tumors (ST) and
are more socially isolated than their peers {[}3, 4{]}. The majority of
studies of social functioning in BT has been cross sectional in nature,
and longitudinal research is needed to better understand the trajectory
and predictors of social functioning in BT over time.

A model of social competence in children with insults to the brain
{[}5{]} integrates risk and resilience factors related to CNS insults,
the family environment, and individual characteristics and offers
direction for research. Insults to the developing brain may impair
cognitive and executive functioning which can in turn lead to poor
social skills and, subsequently, poor social adjustment, including peer
relationships {[}6{]}. Social skills are defined as skills required to
interact appropriately across a variety of social contexts {[}7{]}.
Developmentally inappropriate social skills may cause individuals to
react inappropriately to social situations, in turn leading to peer
isolation and rejection. This model of social competence has been
applied to the BT population {[}8{]} as they experience social late
effects as a result of CNS insult.

Social Information Processing (SIP) is emphasized as a key determinant
of social interaction and social adjustment. Two important elements of
SIP include properly identifying facial expressions and correctly
interpreting others' motivations, also known as theory of mind {[}5{]}.
These are common struggles in youth with Autism Spectrum Disorder (ASD)
{[}9{]} which contribute to difficulties with social interactions
{[}10{]}. If an individual is unable to correctly identify the emotion
of another, it becomes far more difficult to react in a socially
appropriate manner which can lead to social isolation and peer
rejection. The inability to understand when an individual's comments are
sarcastic or ironic can cause someone to misinterpret the speakers'
intent and hinder appropriate social responses. While there is a large
body of research examining these domains of social deficits in youth
with ASD, research in BT is in its inception {[}8{]}. Preliminary
studies have found that BT perform significantly worse than youth with
juvenile rheumatoid arthritis in identifying adult facial expressions
{[}11{]} and that BT with high levels of social impairment were worse at
identifying facial expressions compared to typically developing youth
and youth with ASD {[}12{]}. Longitudinal research is needed to better
understand the social competence of BT over time in order to inform
targeted interventions.

The goal of this longitudinal study was to evaluate important facets of
social competence among ST and BT over time and to identify predictors
of peer relationships. We hypothesized that (a) BT will have worse SIP
and social skills over time compared to ST and that (b) worse SIP and
social skills would predict worse peer relationship quality.

METHODS:

\emph{Participants} :

Participants were youth ages 7-14 who had completed tumor-directed
treatment for either a non-central nervous system (CNS) solid tumor
(n=34) or brain tumor (n=51) within the six months prior to enrollment.
Survivors of pediatric non-CNS solid tumors (ST) were chosen as the
comparison group because they undergo similar treatments and comparable
changes to their daily life during treatment, yet treatment does not
directly affect the brain and they do not tend to show difficulties with
SIP in survivorship. Exclusion criteria included: (1) a multi-systemic
genetic condition affecting cognitive functioning (e.g.,
Neurofibromatosis Type 1, Trisomy 21); or (2) a cognitive or
developmental delay prior to tumor diagnosis. Survivors of non-CNS solid
tumors who completed treatments affecting the CNS (e.g., total body
irradiation) were excluded as well. Caregiver inclusion criteria
consisted of living with the participant at least 50\% of the time,
being fluent in English, and having actively participated in the
participants' cancer treatment.

127 families were approached for this study (n = 72 BT, n = 55 ST) and
83 (65.3\%, n = 49 BT, n = 34 ST) agreed to participate. Reasons for
declining participation included lack of interest (n=22), being too busy
to participate (n=7), and passive refusal (n=15). Two BT were unable to
complete study procedures upon enrollment due to language barriers
resulting in a total sample of 81. There were no differences in
demographic or medical characteristics between consenting and
non-consenting individuals.

\emph{Procedures} :

The current data are from a longitudinal study of social competence in
survivors of pediatric brain and non-CNS solid tumors conducted at a
large, urban pediatric medical center. All procedures were reviewed and
approved by the Institutional Review Board and written informed consent
and child assent were obtained upon enrollment. Potentially eligible
patients were identified through cooperation with medical teams and
tumor registry records. All potential participants were contacted by
study staff via letter, phone, and/or during follow-up visits. This
paper encompasses data from the baseline study visits and the first
follow-up, which occurred approximately 12 months after the baseline
visit. Participants and their primary caregiver were asked to complete
questionnaires (see below) during study visits. Relevant information was
collected via chart review. Participants received a brief feedback
letter and a \$20 gift card as compensation after each study visit.

\emph{Measures:}

Social Information Processing

The Diagnostic Analysis of Nonverbal Accuracy Child Faces 2 (DANVA-2)
{[}13{]} assesses the ability of individuals to properly identify the
facial expressions of children across four emotions (happiness, sadness,
anger, and fear) and two levels of emotional intensity (high and low).
Participants viewed 24 faces and were asked to select the emotion that
they believed was being depicted. The DANVA-2 has established validity
and has been shown to differentiate clinical groups {[}14{]}.

The Literal Truth, Ironic Criticism, and Empathic Praise Task (Irony \&
Empathy) {[}15{]} presents six situations in picture form along with a
recorded narration of the situation (raking a pile of leaves, erasing a
blackboard, making a cake). The narration has neutral, ironic, or
empathic intonation and participants must properly identify the
intention of the narration based on the image and recording. This
measure is frequently used to identify SIP deficits in youth with
traumatic brain injury {[}16{]}.

Social Skills

The Social Skills Improvement System (SSiS) {[}17{]} is a widely-used
parent reported measure of social skills, academic competence, and
problem behaviors. Caregivers rate statements on social skills and
problem behaviors on a scale from 0-3 (0 being never, 3 being almost
always) over the past two months (i.e., expresses feelings when wronged;
starts conversations with peers; gets distracted easily). A standard
score for social skills is calculated where higher scores indicate
better social skills.

Social Adjustment

The Patient-Reported Outcomes Measurement Information System (PROMIS)
Pediatric Peer Relationships-Short Form (PRS-SF) is a validated self and
parent report measure of peer relationships {[}18{]}. Participants rate
eight statements regarding peer relationships on a 0-4 scale (0 being
never, 4 being almost always) over the past seven days (i.e., I felt
accepted by other kids my age, I was able to count on my friends).
Appropriate items are reverse coded to produce a total T score, where
higher scores indicate better peer relationships. The self-report PRS-SF
has demonstrated significant correlations with peer-reported metrics of
social acceptance {[}18{]}.

\emph{Data Analysis Plan}

Linear mixed models were used to evaluate whether (a) BT would have
worse SIP and social skills over time compared to ST and (b) whether
social skills and accuracy in recognizing facial expressions and others'
social intentions were positively associated with peer relationship
quality. For longitudinal designs with two time points and data missing
at random, maximum likelihood estimation used in mixed models produces
less biased estimates than least squares approaches {[}19{]}. Thus, we
used a random intercept model with restricted maximum likelihood
estimation to test our hypotheses. All continuous predictors were
grand-mean centered to aid the interpretation of coefficients.

In the model for hypothesis (a), DANVA-2, Irony \& Empathy, and SSiS
were entered as outcome variables in three separate models, while time,
group and their interaction were entered as predictors. Three models
were run for hypothesis (b) that differed only in terms of the specific
predictor variable tested. The three predictors included baseline values
of SSiS, DANVA-2, and Irony \& Empathy. For example, for the model
evaluating the influence of baseline social skills, PROMIS Pediatric
Peer Relationships was the outcome variable, while time, baseline SSiS,
group and a 3-way interaction between them were entered as predictors.
We also conducted two post hoc analyses in the BT group, where we
evaluated the moderating effect of baseline time-since-diagnosis on
Irony \& Empathy and social skills. Examination of diagnostic plots at
levels 1 and 2 showed that models met assumptions of normality,
linearity, independence and constant variance. The nlme package from the
R Statistical Computing Language was used to run the linear mixed models
and the sjPlot R package was used to produce tables and graphs of simple
slopes.

RESULTS

\emph{Descriptive and Preliminary Analyses}

Baseline visits were completed within six months of completing
tumor-directed treatment (\emph{M} =3.39 months, SD=1.78 months, range =
2 weeks-6.9 months). Time 2 visits occurred an average of 13.1 months
after baseline (SD = 1.72 months, range = 10.3 -- 17.7 months).

Table 1 summarizes the sample's demographic characteristics at baseline.
The majority of BT participants were male (74.5\%), and the majority of
ST participants were female (61.8\%). A majority of both BT and ST were
white (74.5\% and 61.8\% respectively) and non-Hispanic (82.4\% and
73.5\% respectively). The most common treatment modality was surgical
resection only for both BT and ST (33.3\% and 35.3\%, respectively).
Other treatment combinations are provided in Table 1. There were no
differences in age, sex, or ethnicity for participants who only
completed the baseline evaluation versus those who completed both
baseline and follow-up. There was a significant difference in the
ethnicity of BT participants who completed baseline only versus baseline
and follow-up, however this difference is likely explained by relapse
status. Three of the four BT participants who identified as Asian
relapsed or passed away between

Indices of SIP and self-reported peer relationships did not change over
time for either BT or ST. Self-reported peer relationships was in the
average range overall, however 32.6\% of BT had a score one standard
deviation below average versus 15.6\% of ST.

\emph{Hypothesis (a)}

As assessed by DANVA-2 and Irony \& Empathy, BT and ST did not differ in
SIP over time (\emph{b} = -0.00, \emph{se} = 0.01, \emph{t = -}
0.40\emph{p} = .694) and (\emph{b} = -0.01, \emph{se} = 0.06, \emph{t =
-} 0.13 \emph{p} = .896), respectively (Table 2). Similarly, the model
for SSiS failed to show longitudinal differences between BT and ST
(\emph{b =} 1.25, \emph{se =} 2.03\emph{, t =} 0.62, \emph{p =} .542)

\emph{Hypothesis (b)}

The 3-way interaction between time, group and social skills was
significant (Table 3). In the ST group, there was a positive association
between baseline social skills and peer relationships over time (Fig.
1). However, in the BT group, participants with greater social skills at
baseline experienced a decrease in peer relationship quality over time,
while those with lower social skills at baseline experienced an increase
in peer relationship quality over time (Fig. 1).

The 3-way interaction between time, group and Irony \& Empathy was
significant (Table 4). In the solid tumor group, there was a positive
association between baseline Irony \& Empathy and peer relationships
over time (Fig. 2). However, in the BT group, participants with greater
baseline Irony \& Empathy scores showed evidence of a decrease in peer
relationship quality over time, while those with lower baseline Irony \&
Empathy showed evidence of an increase in peer relationship quality over
time (Fig. 2).

The 3-way interaction between time, group, and DANVA-2 was not
significant.

\emph{Post Hoc Analyses}

Post hoc analyses were conducted for the BT group to help contextualize
the unexpected, crossed interaction between baseline Irony \& Empathy
and social skills and peer relationships over time. We examined whether
the crossed interactions varied as a function of time-since-diagnosis,
the intensity of treatment using the Pediatric Neuro-Oncology Rating of
Treatment Intensity (PNORTI) {[}20{]} and treatment risk factors using
the Neurological Predictor Scale (NPS) {[}21{]}. Results showed that the
3-way interaction between time, Irony \& Empathy and
time-since-diagnosis was significant (\emph{b} = -0.04, \emph{se} =
0.01, \emph{t = -} 2.76, \emph{p} = .011), with simple slopes
demonstrating an increase in the crossed interaction between time and
Irony \& Empathy with an increase in time-since-diagnosis. Results
failed to demonstrate a significant 3-way interaction between time,
social skills, and time-since-diagnosis (\emph{b} = -0.00, \emph{se} =
0.00, \emph{t = -} 0.91, \emph{p} = .375). Results also failed to
demonstrate moderating effects of treatment intensity or risk factors
(\emph{b} = 0.33, \emph{se =} 0.17, \emph{t =} 2.00, \emph{p =} .058)
and (\emph{b} = 0.09, \emph{se} = 0.06, \emph{t} = 1.46, \emph{p} =
0.159), respectively.

DISCUSSION

The goal of this longitudinal study was to evaluate components of social
competence, including social information processing, social skills, and
peer relationship quality, over time in survivors of pediatric brain
tumors and non-CNS solid tumors who recently completed treatment. Due to
improvements in survival rates among BT, there is now an emphasis on
understanding their social functioning to better inform what supports
may be needed throughout their lifetime. This is one of the first
longitudinal studies to focus on SIP and peer relationships in BT and
highlights the complexities in how SIP and social skills may relate to
peer relationships in BT over time in comparison to ST. Among ST, we
found positive associations between baseline measures of social skills
and theory of mind and peer relationships over time. Conversely, BT
showed an inverse association between baseline social skills and theory
of mind and peer relationships over time. Those with better social
skills and SIP at baseline had a decline in peer relationships, while
those with worse social skills and SIP at baseline had an improvement in
peer relationships over time. These findings add to a growing area of
research evaluating the importance of social skills in BT {[}5,15{]}.

Our hypothesis that BT would have worse social skills and SIP compared
to ST over time was not supported by the findings. There were no
differences in social skills and SIP over time between these two groups
and, notably, these variables did not change over time for either group.
This could be because study assessments occurred within the first 18
months after treatment completion and may be too early to capture the
neurodevelopmental late effects that arise in BT. A previous study found
that BT who were farther out from end of treatment (3-9 years) showed
significantly poorer face processing skills compared to youth with
Juvenile Rheumatoid Arthritis {[}14{]}. Future longitudinal studies
should follow BT for longer periods of time following treatment
completion to identify when impairments in social skills and SIP
develop.

Across the study, both BT and ST self-reported peer relationship scores
were in the average range. However, the trajectory of self-reported peer
relationship scores over time was affected by both group membership and
baseline theory of mind and social skills. When comparing BT and ST on
peer relationships over time, ST showed relatively stable peer
relationships over time regardless of baseline theory of mind or social
skills. However, for BT, social skills and theory of mind appeared to be
more relevant to peer relationships over time in unanticipated ways.
Face processing was not predictive of peer relationships in BT, which
differs from previous cross-sectional studies which found associations
poor face processing and social functioning {[}12, 22{]}. BT with
significantly lower baseline social skills and theory of mind had
improvements in peer relationships over time whereas BT with
significantly higher baseline social skills and theory of mind had
declines in peer relationships over time. Previous literature has noted
a similar inverse association in processing speed abilities in survivors
of pediatric brain tumors who received radiation therapy with those
scoring the highest having the most marked decline in processing speed
over time {[}23{]}. Moreover, exploratory post-hoc analyses of the
present study suggested that this inverse association is most prominent
in BT who were furthest from diagnosis which was seen in the previously
mentioned study as well. Other factors, such as treatment modalities
(e.g., radiation therapy) and neurological risk, did not affect this
interaction in our analyses. Given that participants were enrolled in
this study within 6 months of completing tumor-directed therapy, further
time since diagnosis may be a proxy for more complex, lengthy treatments
and, therefore, potentially having more sequelae.

Additionally, prior research suggests that BT may overestimate their
social status among peers {[}24{]}. In the current study, participants
rated their own levels of social acceptance by peers using the PROMIS
measure. A potential explanation for these findings is that those with
better baseline theory of mind may have better self-awareness of their
status among peers and more accurately noted their decline in peer
acceptance over time secondary to potential sequelae. Conversely, those
with poorer baseline theory of mind may overestimate their peer
acceptance over time due to difficulty interpreting social cues. Studies
employing peer-reported data would be needed to elucidate these
findings.

This study has several strengths. Data on the social competence of
survivors of pediatric brain and solid tumors upon treatment completion
is relatively limited. Additionally, the longitudinal nature of this
study allows for evaluation of SIP and social acceptance over time to
inform the provision of support services. Lastly, this study utilized a
multi-informant method to evaluate variables of interest in survivors.
Despite these strengths, these data should be viewed in the context of
certain limitations. First, participant attrition led to smaller sample
sizes at time point 2. Retention primarily was affected by participant
relapses and deaths. Second, this study is not racially and ethnically
diverse and findings may not generalize to the population writ large.

This study contributes to the growing body of research on the social
competence of BT {[}14, 25{]} and offers numerous directions for future
research and clinical efforts. Due to the variability in perceived
social acceptance across time points, BT social functioning should be
monitored regularly after the completion of treatment to determine if
and when intervention services would be beneficial. Future research
studies could expand on this work by following survivors for multiple
years post-treatment completion and obtaining peer reports of survivor
social acceptance.

CoI STATEMENT

The authors have no conflicts of interest to report

ACKNOWLEDGEMENTS

This research was supported by the National Cancer Institute of the
National Institutes of Health (K07CA178100). The content is solely the
responsibility of the authors and does not necessarily represent the
official views of the National Institutes of Health. The authors thank
all the participants who provided their time for this study.

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\textbf{Hosted file}

\verb`PBC Table 1_11.23.21.docx`  available at \url{https://authorea.com/users/448535/articles/547337-a-prospective-study-of-social-competence-in-survivors-of-pediatric-brain-tumors}

\textbf{Hosted file}

\verb`PBC Table 2_11.23.21.docx`  available at \url{https://authorea.com/users/448535/articles/547337-a-prospective-study-of-social-competence-in-survivors-of-pediatric-brain-tumors}

\textbf{Hosted file}

\verb`PBC Table 3 11.23.21.docx`  available at \url{https://authorea.com/users/448535/articles/547337-a-prospective-study-of-social-competence-in-survivors-of-pediatric-brain-tumors}

\textbf{Hosted file}

\verb`PBC Table 4 11.23.21.docx`  available at \url{https://authorea.com/users/448535/articles/547337-a-prospective-study-of-social-competence-in-survivors-of-pediatric-brain-tumors}

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