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Mental Health, Sleep, Physical Activity and Family Functioning
in Adolescents with Narcolepsy
by
Arpita Parmar
A thesis submitted in conformity with the requirements
sleep quality, excessive daytime sleepiness, and low PA levels were associated with greater
depression scores. Family functioning was impaired in pediatric narcolepsy patients.
III
Acknowledgements
First and foremost, I would like to thank my supervisor, Dr. Indra Narang for agreeing to
take me on as graduate student and providing me with the opportunity to work with the Pediatric
Sleep and Respiratory Medicine team at The Hospital for Sick Children. I am sincerely grateful
for her endless support, encouragement, guidance and strong mentorship which has been
conducive to my professional and personal growth.
I would also like to express my gratitude towards the members of my program advisory committee
members, Dr. Ann Yeh and Dr. Daphne Korczak, who have provided their expertise, guidance and
support throughout my masters.
Furthermore, I would like to thank Dr. Brian Murray for always being available to provide
his expertise and support with this project. I would also like to thank the sleep clinical team who
facilitated recruitment of the narcolepsy patients (Dr. Shelly Weiss, Dr. Alene Toulany, Dr. Suhail
Al-Saleh, Dr. Reshma Amin, Dr. Kevan Mehta, Dr. Kevin Vezina, Dr. Anya McLaren, Dr.
Saadoun Bin-Hasan, Allison Zweerink and Bridget Doan-Perera). Also a special thanks goes to
Sarah Selvadurai, who personally taught me how to accurately score and analyze actigraphy data,
and provided great support and insight as a fellow graduate student. I would like to acknowledge
members of the sleep research team (Tanvi Naik, Nishtha Pandya and Giorge Voutsas) who have
been helpful, supportive and an overall pleasure to work with. I would also like to give a big thanks
to the adolescents and families who participated in the study. Without these individuals,
conducting this study would have not been possible.
Finally, I would like to thank my family and friends for their unconditional love and support
throughout my Masters and beyond.
IV
Table of Contents
Abstract ........................................................................................................................................................ II
Acknowledgements ..................................................................................................................................... III
Table of Contents ........................................................................................................................................ IV
List of Tables .............................................................................................................................................. VI
List of Figures ........................................................................................................................................... VII
List of Abbreviations ............................................................................................................................... VIII
List of Appendices ...................................................................................................................................... IX
Chapter One: General Introduction ............................................................................................................... 1
(the ability to control and modulate emotions) (Gross, 1998; Palmer & Alfano, 2017). Limited
research from correlational and experimental studies amongst adolescents suggests sleep
deprivation leads to poorer emotional regulation and increased reactivity to negative emotional
stimuli (Baum et al., 2014; McMakin et al., 2016; Vriend et al., 2013). EDS, as a result of sleep
deprivation is also associated with poor-emotional self-regulation in typically developing
adolescents (J. A. Owens et al., 2016).
The relationship between sleep deprivation and disrupted emotional regulation has also
been reported in adults (Palmer & Alfano, 2017). Sleep deprived adults report experiencing
heightened reactivity to negative emotional experiences (Palmer & Alfano, 2017). A study using
functional magnetic resonance imaging in sleep deprived adults showed, greater activation of the
amygdala in response to negative stimuli compared to adults who were not sleep deprived (Yoo et
al., 2007). This study also showed decreased connectivity between the medial prefrontal cortex
and the ventral anterior cingulate cortex in sleep deprived adults, which can weaken emotional
control (Yoo et al., 2007).
Interestingly, preliminary data suggests that adolescents may be even more susceptible to
the emotional effects of sleep deprivation than adults (McGlinchey et al., 2011) because they are
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still developing emotional regulation skills (J. A. Owens et al., 2016). Regions of the brain that
govern emotional regulation (the prefrontal cortex, amygdala and ventral anterior cingulate cortex)
are still undergoing developmental changes during adolescence (Casey, 2015), and sleep
deprivation may adversely affect their normal function (Holm et al., 2009; Telzer, Fuligni,
Lieberman, & Galvan, 2013).
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6.2.3 Physical Activity in Pediatric Narcolepsy
This thesis was the first to evaluate PA levels in the pediatric narcolepsy population. Daily
step count between the narcolepsy and control group were not significantly different. However,
both groups had lower PA levels than the recommended daily 10 000 to 15 000 steps for
adolescents (Tudor-Locke & Bassett, 2004). This is consistent with results from the 2012 to 2013
Canadian Health Measures Survey showing that over 90 per cent of children and adolescents (ages
5–17 years) do not meet Canada’s recommended guideline of 60 minutes of moderate-to-vigorous
PA daily (Canada, 2015). The lack of PA seen in both groups of adolescents may be due to
competing demands (e.g., school work, extracurricular commitments) taking time away from PA
(Bauer, Yang, & Austin, 2004).
Objective PA levels in this group of adolescents with narcolepsy are similar to findings
from the adult narcolepsy population (Matoulek et al., 2017). One study on adults with narcolepsy
(n=42, mean age 34.9 ± 10.0) reported patients had a low average daily step count of 6346 ± 2026
(Matoulek et al., 2017) which is similar to this cohort of adolescents with narcolepsy. Lower PA
levels in narcolepsy may also be associated with low cardiopulmonary fitness, which has been
reported in the adult narcolepsy population (Matoulek et al., 2017). PA levels may also be lower
in adolescents with narcolepsy because of decreased spontaneous activity levels (Bruck et al.,
2005). Decreased spontaneous activity has been reported in adults with narcolepsy, even when
treated with stimulants (Bruck et al., 2005).
Even though adolescents in both groups had low objective PA levels, the vast majority of
participants self-reported PA levels to be in the ‘active’ range (Godin health contribution score
>24). This discrepancy between objective and self-report data may be due to bias seen with self-
report measures (e.g., over estimating PA levels) (Prince et al., 2008). Additionally, some
adolescents may have taken off the pedometer during certain types of aquatic PA (e.g., swimming),
or simply did not wear the device whilst partaking in PA. Although both groups of adolescents
self-reported high PA levels, a significantly lower percentage of adolescents in the narcolepsy
group were in the active range compared to the control group (73.3 vs 93.3 per cent; p=0.04). It
can be speculated that adolescents in the narcolepsy group self-reported lower PA levels, because
they feel that the symptoms of their condition (e.g., EDS, cataplexy) make it more difficult for
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them to participate in PA. Godin health contribution scores in adolescents with narcolepsy (47.3 ±
31.7) are similar to other adolescents with neurological disorders such as monophasic acquired
demyelinating syndrome (54.0 ± 49.0) and multiple sclerosis (40.0 ± 46.0), who report symptoms
of fatigue from lack of sleep, as well as depression (Grover et al., 2015)
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6.2.4 The Association between Physical Activity, Sleep Patterns and
Depressive Symptoms
This thesis also evaluated the association between depression scores and PA levels in
adolescents with narcolepsy and controls. In adolescents with narcolepsy, self-reported and
objective PA levels were associated with depression scores. However, this association was not
seen in the control group, which is in contrast to larger studies in healthy adolescents where an
inverse association between PA levels and depression scores have been reported (Biddle & Asare,
2011) (Kremer et al., 2014; Wiles et al., 2012). This association may have not been seen in control
group of this study due to the small sample size (n=30).
The association between increased PA levels and lower depression scores may be
explained through a biological mechanism, specifically how participating in PA releases
endorphins, which are associated with feelings of euphoria (Dishman & O'Connor, 2009; Lubans
et al., 2016). Euphoric feelings after participating in PA may be due to changes in one or more
brain monoamines, with the strongest evidence available for dopamine, noradrenaline, and
serotonin (Lin & Kuo, 2013; Lubans et al., 2016). However, further research is needed to support
this assertion in pediatric populations (Bouix et al., 1994; Lubans et al., 2016).
The association between increased PA levels and lower depression scores may also be
explained through psychosocial pathways. Participating in PA in group settings may provide
adolescents with opportunities for social interaction and peer-conformity, and consequently
improve mood (Wiles et al., 2012). The relationship between PA and depression scores may also
be bidirectional (Korczak et al., 2017). It can be speculated that adolescents with narcolepsy may
not be interested in participating in PA because of co-existing depressive symptoms, which
encompass low mood and self-esteem. It can also be speculated that adolescents with narcolepsy
may avoid participating in PA such as team sports, because of the symptoms of their condition
(e.g., episodes of cataplexy), which occur unexpectedly and may be embarrassing (Matoulek et al.,
2017).
In the narcolepsy group, greater self-reported PA levels were also associated with and
better self-reported sleep quality. The association between PA and improved sleep quality has been
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reported amongst adolescents with obesity (n=20; mean age: 14.5 ± 1.5 years; body mass index:
34.0 ± 4.7 kg/m2) who participated in a 12-week exercise-training program (3 hours of
exercise/week) (Mendelson et al., 2016). In this study, PSG data showed an increase in sleep
efficiency from baseline (+7.6 per cent; effect size: 0.76; p = 0.028) (Mendelson et al., 2016).
The relationship between PA and sleep quality may be attributed to the increase in deep
sleep (NREM-3) that has been associated with participating in regular PA (Driver & Taylor, 2000).
One study reports that healthy adolescents who participate in PA for 3.5 hours per week spend a
greater percentage of total sleep time in NREM-3 sleep compared to adolescents who engage in
PA for less than 3.5 hours per week (37.4 ± 6.4 vs 29.3 ± 4.3 per cent of total sleep time; p<0.001)
and have a greater sleep efficiency (95.19 ± 3.68 vs 94.72 ± 3.91 per cent; p<0.05) (Brand et al.,
2010). Additionally, an experimental study in healthy adult males (mean age 27.1 ±1.3 years) has
shown that sleep deprivation reduces free-living PA (Schmid et al., 2009), so it can be speculated
that feeling more rested (from having better sleep quality) may allow adolescents to have more
energy to participate in PA.
Surprisingly, there was no association between EDS and PA levels (both objective and
self-reported) in adolescents with narcolepsy, for reasons that are unclear. Although of PA has
been recommended for patients with narcolepsy to improve wakefulness due to its stimulating
effect (K. Maski & Owens, 2016), evidence for this statement is lacking. There were also no
associations seen between total sleep duration (measured by actigraphy) and PA levels. This may
be because of pedometers were used as an objective measure of PA, which are unable to assess
PA intensity. In the two studies assessing objective PA and sleep amongst healthy adolescents, an
accelerometer was used to assess PA (Lang et al., 2013) (Gerber et al., 2014). Both studies reported
that greater PA intensity is associated with longer sleep duration (Lang et al., 2013) (Gerber et al.,
2014).
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6.2.5 Family Functioning in Pediatric with Narcolepsy
PedsQL family impact module total, communication and worry subscale scores in this
cohort of adolescents with narcolepsy were significantly lower than a community sample not
seeking ongoing care for a medical condition (Medrano et al., 2013). PedsQL family impact
module total scores may be significantly lower in the narcolepsy group compared to a community
sample because of the greater burden associated with caring for a child with a medical condition,
leaving less time for enjoyable activities (McClellan & Cohen, 2007).
PedsQL family impact module total, parent HRQOL, family summary worry and
communication scores in the narcolepsy group were significantly lower than the traumatic brain
injury group (e.g., skull/brain trauma, concussions) (de Kloet et al., 2015). PedsQL family impact
module total scores may be significantly lower in the narcolepsy group compared to children and
adolescents with traumatic brain injuries for various reasons. Firstly, pediatric narcolepsy is more
rare than pediatric traumatic brain injury, and rare diseases receive less public awareness and
support from health care teams as information on disease progression is limited (Dharssi, Wong-
Rieger, Harold, & Terry, 2017). Lack of support and disease awareness may cause patients their
families to feel misunderstood and isolated, which negatively impacts overall family functioning
(Kippola-Paakkonen et al., 2016). Parents of pediatric patients with narcolepsy have reported
relying on support from close family and friends, and that support from health care professionals
is less common (Kippola-Paakkonen et al., 2016). Secondly, the disease course of narcolepsy
varies greatly from traumatic brain injury. Narcolepsy is a chronic condition with no cure,
unpredictable symptoms and limited treatment options (Kiran Maski et al., 2017). In contrast, a
traumatic brain injury is the result of an acute adverse event, where the patient is recovering to a
point where they may eventually lead the life of a healthy child (de Kloet et al., 2015). PedsQL
Family Impact Module total scores in the narcolepsy group are similar to a pediatric chronic pain
population, who experience a similar disease course of no cure, unpredictable symptoms and
limited treatment options (Jastrowski Mano et al., 2011).
Scores in the worry domain of the PedsQL Family Impact Module were the lowest of all
domains, and significantly lower than families with a traumatic and non-traumatic brain injury (de
Kloet et al., 2015). The worry domain asks caregivers questions regarding anxiety about medical
treatments efficacy, treatment side-effects, others reacting to their child’s illness, illness affecting
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other family members and their child’s overall future (Varni et al., 2004). The low scores in the
worry domain may be because caregivers of children with non-curative chronic conditions often
experience a profound uncertainty with respect to their child’s future (Bally et al., 2018).
Caregivers of children with chronic conditions have described feeling fearful, alone and powerless
about their child’s diagnosis and ambiguity about their future health or overall future (Bally et al.,
2018). It can be speculated that families with narcolepsy may worry about daily symptoms (e.g.,
EDS and cataplexy) interfering with productivity in the school setting, which would limit future
educational opportunities (e.g., going to university) and further employment prospects. Parents of
pediatric patients with narcolepsy have also reported worrying about the lack of resources available
to help their child and their family in coping with the illness (Kippola-Paakkonen et al., 2016).
Family summary scores, which assess how daily activities and family relationships are
affected by an illness (Varni et al., 2004), were also significantly lower than families with a
traumatic brain injury (de Kloet et al., 2015). Caring for a child with a chronic condition may also
put greater demands on a caregiver like taking time off work to take their child to routine clinic
appointments, administering medication to their child which may impede daily routines (Herzer et
al., 2010). Added stress and workload may also cause tension between family members, as one
caregiver may feel a greater burden if responsibilities are not evenly distributed between parents
(Herzer et al., 2010). Daily activities may require more effort and flexibility in families caring for
a child with a chronic condition (Herzer et al., 2010). For example, in narcolepsy, caregivers may
find it more challenging to get their child up and ready for school, due to sleep fragmentation and
subsequent early morning fatigue.
These findings highlights how important it is for health care professionals to provide
family-centered care to patients with narcolepsy. This can be also done in collaboration with
services that offer support to the family (e.g., social work, child life specialists) who need to
understand specific needs of the family and connect them to the appropriate resources (e.g.,
community centers with activities for the entire family).
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6.3 Strengths and Limitations
This is the first study to evaluate and describe the relationship between sleep patterns, PA
levels and depression and anxiety scores amongst adolescents with narcolepsy. This study also
provides preliminary findings regarding the predictors of depression scores amongst adolescents
with narcolepsy. Furthermore, this study uses both objective and self-report measures to assess
sleep patterns and PA levels. Lastly, a control group was a part of the study to assess how having
a diagnosis of narcolepsy affects sleep patterns, PA levels and depression scores.
However, this study has several limitations that require consideration. The sample size of
the study population was small, and further large scale studies are needed to confirm these results.
Also this study was powered to evaluate and compare the differences in depression scores (CDI-2
total scores) between adolescents with narcolepsy and controls, and not powered to evaluate if
sleep patterns, EDS and PA levels are associated with depression scores.
The participants in this study were predominately male, so gender-specific effects of sleep
patterns, PA levels and depression and anxiety scores could not be evaluated. Additionally,
females typically report higher depression scores than males, so it is possible that depressive
symptoms were under-represented in this cohort. We also did not match the control group for age
and sex due to limited availability of participants. There was also a statistically significant
difference between ages between the control group and the narcolepsy group where the control
group was approximately one year older (14.9±1.5 vs 13.8±2.2 years; p=0.03) and being of older
age has been reported to be associated with higher depression scores (Saluja et al., 2004). However
the mean age of both groups were within a year of each other and limited to the early teen years.
Also, the observational nature of this study may introduce a potential for bias, as variables such as
sex, age and the presence of co-existing obesity have been reported to be associated with the
exposure variables (sleep patterns and PA levels) as well as the primary outcome (depression
scores). Additionally, it is likely that there are bidirectional relationships between the exposure
and outcome variables in this thesis, which could not be assessed because data was only collected
at one time point. Furthermore, it is unclear if patients had depressive symptoms/anxiety prior to
their narcolepsy diagnosis as this data was not available. Additionally, depressive symptoms and
anxiety were assessed by patient-report measures in this study and not through clinical interviews
by a child and adolescent psychiatrist. Clinical interviews are necessary to identify external factors
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(e.g., bullying, parents divorcing) that may contribute to depressive symptoms. The patient-report
measures have been validated in pediatric populations, but not in patients with narcolepsy.
Moreover, actigraphy estimates sleep-wake cycles based on gross motor activity, but
cannot differentiate sleep stages which can only be done using PSG. However, PSG can be
burdensome for adolescents and their families, which could potentially influence recruitment bias.
Also, PSG only provides information about sleep patterns on one night and are not performed in
an adolescent’s natural sleeping environment. Another limitation was the use of pedometers for
assessment of PA levels. Pedometers only provide a step count and do not describe the level of
intensity PA was performed at. Future research on PA levels amongst adolescents with narcolepsy
should consider the use of an accelerometer, to assess PA intensity. Also there may have been
reporting bias in the pedometer tracking log, where the participant stated they wore the device
throughout the day when they actually did not. Moreover, the use of self-report measures for PA
may introduce recall and response bias, as patient may over/under estimate how much PA they
participate in for reasons such as inaccurate memory and social desirability (Prince et al., 2008).
Finally, using secondary data analyses for the comparison between family functioning scores is
also a limitation, as group differences could only be evaluated in the studies that reported mean
and standard deviation values of scores.
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6.4 Future Directions for Research
Future research is needed to confirm and build on the findings of this study. Longitudinal
studies assessing depressive symptoms from the time of disease onset throughout adolescence and
adulthood is important to understand when depressive symptoms and anxiety begin and how they
change over time. Longitudinal studies may also be useful in assessing the direction of the
association (e.g., bidirectional) between sleep patterns, PA levels and depressive symptoms. It is
also important to assess other factors that may be associated with depressive symptoms, such as
pathophysiological features of narcolepsy (e.g., amount of time spent in REM sleep, hypocretin
levels). Future studies should also include a qualitative component with structured interviews
where adolescents with narcolepsy discuss how the condition impacts their mental health and
psychosocial functioning, and the type of support they would like to receive from their caregivers
and health care teams. Qualitative research can also be useful in understanding barriers adolescents
with narcolepsy face to participating in PA. Finally, this thesis identified many patients with
elevated depression and anxiety scores, so patients were refereed on to services from adolescent
medicine and child psychiatry for additional support. It would be interesting to assess what affect
these services had on depressive symptoms and anxiety amongst adolescents with narcolepsy, and
what strategies (e.g., pharmaceuticals, behavioural intervention) were most beneficial to patients.
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