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Journal of Anxiety Disorders 85 (2022) 102514

Contents lists available at ScienceDirect

Journal of Anxiety Disorders


journal homepage: www.elsevier.com/locate/janxdis

Comparing symptom networks of daytime and nocturnal panic attacks in a


community-based sample
Nicole S. Smith *, Brian W. Bauer, Daniel W. Capron
Department of Psychology, University of Southern Mississippi, Hattiesburg, MS, USA

A R T I C L E I N F O A B S T R A C T

Keywords: Nocturnal panic refers to waking in a state of panic without obvious triggers, experiencing the same symptoms as
Nocturnal panic panic attacks that occur while awake. Interrelationships between daytime and nocturnal panic symptoms have
Network Analysis not been examined despite theories suggesting panic symptoms perpetuate one another in a forward feedback
Panic symptoms
loop. The current study compared associations between symptoms in daytime and nocturnal panic using network
Sleep
Anxiety
analysis. Network theory conceptualizes symptoms as causing one another, rather than originating from a latent
variable (i.e., a disorder). Given that nocturnal panic originates from sleep stages without cognitive activity,
cognitive symptoms were expected to be more central in daytime panic networks than nocturnal panic networks.
Prior literature indicates similar nocturnal and daytime panic severity; thus, we expected that panic groups
would report equivalent panic symptom severity. An online community sample (N = 215) provided panic
symptom history. Panic network structures did not differ, although the daytime panic network produced stronger
and more numerous connections between physical and cognitive symptoms. The nocturnal panic group, how­
ever, reported more severe cognitive symptoms than the daytime panic group. These results challenge
biologically-focused nocturnal panic theories and suggest a more significant role of cognitive symptoms in
perpetuating nocturnal panic attacks once the individual awakens.

1. Introduction have shown that although the same symptoms occur in both nocturnal
and daytime panic, individuals report a greater number of physical
Nocturnal panic refers to panic attacks that begin while an individual symptoms such as increased heart rate, chest pain, and smothering
is sleeping and result in awakening in the midst of a panic attack (Freed, sensations during nocturnal panic compared to daytime panic attacks
Craske, & Greher, 1999). Nocturnal panic attacks occur specifically (Craske & Barlow, 1989; Craske & Kreuger, 1990; Norton, Norton,
during the transition between light sleep (Stage II) and deep sleep (Stage Walker, Cox, & Stein, 1999). Similarly, catastrophic cognitions such as
III), in the absences of external triggers such as nightmares and sudden fear of dying or going crazy appear to be more strongly related to day­
noises (Craske & Rowe, 1997). For this reason, nocturnal panic has often time panic than nocturnal panic (O’Mahony & Ward, 2003). These
been conceptualized as a purely biological panic attack that occurs findings support the conceptualization of nocturnal panic as a
without precipitating cognitive factors (Craske & Rowe, 1997; Labbate, biologically-driven panic event, therefore challenging the assumptions
Pollack, Otto, Langenauer, & Rosenbaum, 1994; Shapiro & Sloan, 1998). of cognitively-driven panic theories (e.g., Clark, 1988; Schmidt, Lerew,
Panic theories to date have relied heavily on cognitive influences to & Trakowski, 1997).
explain panic attacks without accounting for nocturnal panic (see review Importantly, the literature on whether nocturnal and daytime panic
by Bouton, Mineka, & Barlow, 2001). differ in severity remains inconclusive. For example, Craske and Barlow
The extant literature suggests that panic attacks comprise the same (1989) found that daytime panic symptoms were rated as more severe
symptoms regardless of if they occur out of sleep (nocturnal panic) or than nocturnal panic symptoms within a Panic Disorder sample. Krystal,
while awake (daytime panic; Freed et al., 1999; Uhde, 1994). Subtle Woods, Hill, and Charney (1991), however, found no differences in the
differences in the strength and frequency of these symptoms may help number, severity, or duration of panic symptoms between nocturnal and
better characterize and understand nocturnal panic. Several studies daytime panic groups. Finally, de Beurs et al. (1994) found that

* Correspondence to: Department of Psychology, University of Southern Mississippi, 118 College Drive #5025, Hattiesburg, MS 39406, USA.
E-mail address: nicole.s.smith@usm.edu (N.S. Smith).

https://doi.org/10.1016/j.janxdis.2021.102514
Received 5 April 2021; Received in revised form 31 October 2021; Accepted 6 December 2021
Available online 9 December 2021
0887-6185/© 2021 Elsevier Ltd. All rights reserved.
N.S. Smith et al. Journal of Anxiety Disorders 85 (2022) 102514

nocturnal panic attacks were rated as more severe than daytime panic They proposed that learned high arousal schemas lead to panic attacks
attacks. A more nuanced examination of which panic symptoms are in response to normal variations in physiological symptoms through
reported as characteristic of daytime and nocturnal panic may be positive feedback loops. These positive feedback loops are believed to
necessary to fully understand the differences between these types of consist of conditioned threat responses to interoceptive stimuli that
panic attacks. occur in the absence of ongoing cognitive appraisals. Robinaugh et al.
Panic symptoms may perpetuate one another differently depending (2020) then used network analysis to illustrate changes in panic disorder
on whether an individual is asleep or awake when the panic attack be­ symptoms throughout treatment but did not include individual cogni­
gins. The body vigilance model has been used to describe maintaining tive and physical symptoms reported by participants as characteristic of
factors for daytime panic in panic disorder and identifies attention to their panic attacks. Instead, physical symptoms were combined into one
physiological changes as a key element to the forward feedback loop node and cognitive symptoms were combined into another node to be
that triggers panic attacks (Schmidt et al., 1997). In this model, cogni­ assessed in relation to avoidance behaviors, escape behaviors, and
tive factors such as scanning the body for physiological fluctuations and emotional responses (Robinaugh et al., 2020). Network analysis repre­
fear of arousal symptoms occur prior to physical panic symptoms. For sents an opportunity to examine the interactions between specific
nocturnal panic, however, researchers have argued the reverse, where physical and cognitive panic symptoms in nocturnal and daytime panic
nocturnal panic physical symptoms occur first, during sleep, and are attacks for the first time, and to compare the central nodes of those
followed by cognitive symptoms after the individual awakens (Craske & networks to one another.
Freed, 1995). Uhde (1994) proposed a forward feedback mechanism for
nocturnal panic where a spontaneous nocturnal panic event leads to 1.1. Aims and hypotheses
anticipatory anxiety in the future out of fear of additional nocturnal
panic attacks. This fear then leads to a more general fear of sleep and The current study expands on extant literature addressing nocturnal
sleep avoidance, resulting in chronic lack of sleep which worsens panic panic attacks compared to panic attacks that occur from a wakeful state.
and anxiety symptoms, ultimately leading to more frequent nocturnal This study is the first to use a network analysis approach to visualize and
panic. Indeed, individuals who experience regular nocturnal panic at­ compare symptom clusters between nocturnal and daytime panic at­
tacks report difficulty returning to sleep after a nocturnal panic attack tacks. This study will further extend the literature by using equivalence
out of fear of additional panic attacks (Tsao & Craske, 2003) and are testing to determine if nocturnal and daytime panic attacks are experi­
more likely than individuals who only panic while awake to report enced as equally severe. We predict that nocturnal and daytime panic
sleeping fewer than 5 hours per night (Singareddy & Uhde, 2009). symptom reports will produce significantly different network structures,
Because nocturnal panic occurs during the transition between light sleep with nocturnal panic attacks having more central physical symptom
and deep sleep, in the absence of conscious thought, it is unlikely that nodes and daytime panic attack having more central cognitive symptom
cognitive panic symptoms are responsible for triggering nocturnal panic nodes. We also predict that nocturnal and daytime panic attacks will be
attacks, though they may play a role in triggering daytime panic attacks. rated as equally severe. We expect these patterns to hold both when
The relations among symptoms reported as occurring during a comparing individuals who panic only while awake (daytime panic
typical panic attack has been an understudied topic. Network analysis is group; DP) to those who panic while awake and out of sleep (nocturnal
a statistical approach that provides the unique opportunity to depict panic group; NP) as well as when comparing daytime and nocturnal
how panic symptoms interact with one another. In the network theory of panic attacks within the NP group. Lastly, we predict that physical
psychopathology, symptoms have causal interactions with one another symptoms will be rated as more severe by the NP group whereas
rather than being caused by an underlying latent variable (McNally, cognitive symptoms will be rated more severe by the DP group.
2016). Thus, the result of the interrelations between symptoms is the
disorder itself. This is in contrast to the medical model in which an 2. Methods
underlying disease causes the observed symptoms (Borsboom, 2017).
Network theory posits that mental disorders consist of clusters of 2.1. Participants
symptoms that co-occur for unknown reasons, resulting in unsuccessful
searches for a single common cause of any mental disorders (Borsboom, Participants (N = 215) were adults recruited for two online studies
2017). For example, in panic disorder the panic attacks cause worry examining anxiety and sleep disturbances (Smith, Martin, Bauer, Ban­
about future panic attacks as well as behavioral changes to avoid panic del, & Capron, 2020; Smith & Capron, 2020). Inclusion criteria for both
attacks (Borsboom & Cramer, 2013). Network theory would assert that studies required participants to be at least 18 years of age, living in the
there is no latent construct causing avoidance, worry, and panic attacks United States, and able to read English fluently. Participants were
separately (Borsboom & Cramer, 2013). Similarly, within a panic attack divided into nocturnal panic (NP), daytime panic (DP), and without
symptoms are thought to have causal influences over one another (e.g., panic (WP) groups based on self-report of panic attack history. In­
shortness of breath causing dizziness which in turn causes fears of losing dividuals from the WP group were not included in the current study’s
control). analyses. Participants who endorsed having at least one past nocturnal
In a network analysis, symptoms are represented as “nodes” and panic attack comprised the NP group (N = 107) regardless of whether or
connections are represented by lines called “edges.” From this not they also endorsed a history of daytime panic attacks. Ninety-five
perspective, the most central nodes (i.e., symptoms) of the network exert participants endorsed both daytime and nocturnal panic attacks
the most influence over the rest of the symptoms and are hypothesized to (88.8% of NP) and 12 participants endorsed only nocturnal panic attacks
be of most theoretical and clinical interest (Freeman, 1978). Thus, in the with no history of daytime panic attacks (11.2% of NP). Participants
case of daytime and nocturnal panic attacks, the centrality of physical who endorsed having at least one past daytime panic attack and no
versus cognitive symptoms in each network may reveal new information history of nocturnal panic attacks comprised the DP group (N = 108).
about the panic experiences in relation to one another. Some research, Fifty-six NPs and 52 DPs were recruited through Amazon’s Mechanical
however, has indicted that factors beyond centrality may be important Turk (MTurk) system and had an approval rating of 95% or higher. The
to consider such as the point at which the symptoms develop in the remaining participants were recruited through a Southeastern uni­
course of the disorder, transdiagnostic factors for comorbid disorders, versity’s online student participant pool.
and resilience factors (Fried et al., 2017). A stringent screening process was used to account for difficulties in
To our knowledge, network analysis techniques have yet to be used differentiating panic attacks from sub-clinical anxiety in self-report data.
to characterize panic attack symptoms. Robinaugh et al. (2019) have Participants were excluded if they endorsed having had a nocturnal or
suggested that panic attacks may be viewed from a network perspective. daytime panic attack but failed the corresponding panic attack

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N.S. Smith et al. Journal of Anxiety Disorders 85 (2022) 102514

definition check. The definition checks for both nocturnal and daytime 2.3. Measures
panic required that the participants choose the correct description from
four alternatives containing distractor options that are commonly 2.3.1. Nocturnal Panic Screen
confused with panic (e.g., feelings of nervousness, waking from a The Nocturnal Panic Screen (Craske & Tsao, 2005) is an 18-item
nightmare). Participants were also excluded if they endorsed having had measure used to assess an individual’s history of nocturnal panic at­
a nocturnal or daytime panic attack but denied ever experiencing four or tacks regarding frequency, symptom severity, and timeline (e.g., When
more panic symptoms during a single panic attack, as required by DSM-5 was your most recent panic attack from a sleeping state?). The online
criteria (APA, 2013). No demographic differences were found when version of the screener provides a detailed description of a nocturnal
comparing those included and excluded from analyses. panic attack displayed at the top of the screen so that participants may
Participants ranged in age from 18 to 67 (M=28.4, SD=10.5) and easily differentiate nocturnal panic from other nighttime awakenings (e.
were mostly female (N = 152; 70.7%). The majority of participants g., nightmares, sudden noises). Participants provide severity ratings for
identified their race as White (70.2%) with the rest of the sample the fourteen panic symptoms listed in the DSM-5 on a 5-point Likert
identifying as Black/African American (13.0%), Latinx (7.0%), Bi-racial scale (ordinal variables) ranging from 0 (Not at all) to 4 (Extreme) based
(7.0%), Asian (2.3%), or American Indian (0.5%). Demographic char­ on their typical experience of recent panic attacks. Participants rated the
acteristics of panic groups are reported in Table 1. Participants in the NP severity of ten physical symptoms (e.g., shortness of breath, dizziness)
group were more likely to identify as Bi-racial (11.3%), to have served in and four cognitive symptoms (e.g., detached or unreal feelings, fears of
the military (14%), to have a disability (17.8%), and to identify as going crazy). The final item on the online version of the Nocturnal Panic
transgender (10.3%). Participants in the DP group were more likely to Screen is a definition check used to ensure that participants could
identify as Black/African American (17.6%). correctly identify a nocturnal panic attack from a set of distractors
commonly confused with nocturnal panic. In this sample, the symptom
severity ratings of the nocturnal panic screener had good reliability (ω =
2.2. Procedure 0.87, 95% CI:.84–0.91).

Participants who met the eligibility criteria completed self-report 2.3.2. Daytime Panic Screen
questionnaires online. Please refer to the original studies (Smith et al., The Daytime Panic Screen mirrors the structure and wording of the
2020; Smith & Capron, 2020) for specific procedures. All procedures for Nocturnal Panic Screen (described above). It is a 19-item measure that
both studies received approval from the university’s Institutional Re­ assesses the frequency, symptom severity, and timeline of daytime panic
view Board. All participants provided informed consent prior to data attacks (e.g., Have you ever experienced a panic attack while awake?). In
collection. addition to the items included in the Nocturnal Panic Screen, the Day­
time Panic Screen also contains an item concerning unexpected daytime
Table 1 panic attacks (e.g., Have you ever experienced a panic attack while awake
Demographic characteristics by group. that occurred for no apparent reason or “out of the blue”?) The online
Nocturnal Panic Daytime Panic version of this screener provides a detailed description of a daytime
Percentage Percentage χ2 panic attack displayed at the top of the screen so that participants may
Biological Sex easily differentiate daytime panic from other forms of anxiety. Partici­
Female 68.2% 73.1% 52 pants report severity ratings for the fourteen panic symptoms listed
Race 04 * above on a 5-point Likert scale (ordinal variables) ranging from 0 (Not at
White 72.0% 68.5%
all) to 4 (Extreme). The final item on the online version of the Daytime
Black/African American 8.4% 17.6%
Latinx 6.5% 7.4%
Panic Screen is a definition check used to ensure that participants could
Asian 9% 3.7% correctly identify a daytime panic attack from a set of distractors
American Indian 9% 0% commonly confused with panic. In this sample, the symptom severity
Bi-racial 11.3% 2.7% ratings of the daytime panic screener had good reliability (ω = 0.89,
Marital Status 10
95% CI:.86–0.91).
Never married 65.4% 77.8%
Married 26.2% 13.9%
Divorced 8.4% 7.4% 2.4. Data Analytic Plan
Widowed 0% .9%
Education 31
We performed the network analyses in four main steps: 1) Network
High school diploma 15.0% 21.3%
Some college, no degree 41.1% 32.4% estimation; 2) Network inference; 3) Network stability; and 4) Network
College Degree 43.9% 45.4% comparison. All data analyses were performed using R version 4.0.3 (R
Employment status 44 Core Team, 2020) and we used the R package qgraph (Epskamp, Cramer,
Unemployed 28.0% 36.1% Waldorp, Schmittmann, & Borsboom, 2012) to visualize networks. A full
Employed part-time 25.2% 25.0%
Employed full-time 45.8% 38.9%
list of packages can be found in the Supplemental Material. Study var­
Military Status 02 * iables were normally distributed. Missing data were handled using the
Not a veteran 86.0% 97.2% MICE package v. 3.8 in R (Van Buuren & Oudshoorn, 2020).
Veteran 6.5% .9%
Active duty 6.5% .9%
2.4.1. Network estimation
Reserve 9% .9%
Disability 17.8% 5.6% 01 * To examine the network structure of panic symptoms between DP
Sexual Orientation 68 and NP, we estimated two independent Gaussian Graphical Models (i.e.,
Heterosexual 73.8% 82.4% regularized partial correlation network) using the qgraph package
Homosexual 2.8% 1.9% (Epskamp et al., 2012). The Gaussian Graphic Models (GGM) is a reg­
Bisexual 20.6% 13.9%
Asexual 9% .9%
ularization technique that retrieves a sparse network where spurious
Pansexual 9% .9% edges are removed (Epskamp & Fried, 2018), and is encouraged when
Transgender 10.3% .9% 01 * assessing psychological networks with smaller sample sizes (Epskamp,
Age Kruis, & Marsman, 2017). In GGM, if two symptoms are connected, they
Mean (SD) 28.6 (10.9) 28.1 (10.2) p = .68
form an edge indicating that symptoms may be conditionally dependent
Note. Nocturnal Panic N = 107. Daytime Panic N = 108. * p < .05. upon one another after controlling for all other symptoms. We used the

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N.S. Smith et al. Journal of Anxiety Disorders 85 (2022) 102514

Graphical Least Absolute Shrinkage and Selection Operator (gLASSO; 2018). Lastly, as other authors have noted (e.g., (Vervaet, Puttevils,
Friedman, Hastie, & Tibshirani, 2014) with Extended Information Cri­ Hoekstra, Fried, & Vanderhasselt, 2021)), cutoffs for interpreting
terion model selection (EBIC; Luo & Chen, 2014; γ = 0.5) to estimate two edge-weight accuracy through bootstrapped confidence intervals is
individual networks (i.e., DP, NP). currently missing in the literature.
The Fused Graphical Lasso (FGL) was used to estimate a joint We assessed the stability of the order of the centrality indices by
network (Danaher, Wang, & Witten, 2014). The FGL extends gLASSO by using a case-dropping subset bootstrap, where nodes that remain
applying an additional penalty to differences among corresponding edge centralized in an estimated network after random subsets of participants
weights in networks using differing samples. Overall, FGL improves are removed, it suggests stability of the order of centrality estimates. For
network estimates by neither suppressing differences or increasing this, we report the correlation stability coefficient that represents the
similarities across groups. Optimal values and parameters were selected proportion of participants that can be removed to retain a correlation of
by using a k-fold cross-validation using the EstimageGroupNetwork ≥ 0.7 between the centrality order of the bootstrapped datasets and the
package (Costantini & Epskamp, 2017). Networks were plotted using the full dataset or the bootstrap edge weights and the original edge weights
Fruchterman-Reingold’s algorithm (Fruchterman & Reingold, 1991), (with 95% probability). According to Epskamp and colleagues (2018),
where more strongly related nodes hold central positions. The strength the centrality stability coefficient should be > 0.25 and preferably ≥
of the associations is reflected visually by the thickness of the edges 0.50.
whereas the valence (i.e., positive, negative) connections between nodes
is depicted by edge color. The maximum absolute edge weight was set at 2.4.4. Network difference estimation
“1.0′′ and graph layouts were fixed allow comparison between the two To evaluate potential difference in network structure between panic
network graphs. groups, we performed two analyses. First, we investigated the similarity
of the two networks by correlating their adjacency matrices, the pre­
2.4.2. Network inference dictability nodes, and the centrality indices. Correlation coefficient
To identify nodes that were most influential in the 14-item panic strength from + /− 0.1 to.3 were considered weak, + /− 0.3 to + /− 0.6
symptom network, we estimated expected influence (Robinaugh, Mill­ moderate, and + /.7 or above was conserved strong (Dancey & Reidy,
ner, & McNally, 2016) rather than strength. Expected influence is the 2007). Second, we used permutation tests for connectivity invariance
sum of all edges of a node and takes into account both positive and and network structure invariance to determine potential differences
negative edges. This is in contrast to using the absolute sum of all edges between the networks using the NetworkComparisonTest package (van
(i.e., node strength), which may distort interpretation. Further, recent Borkulo, Epskamp, Jones, Haslbeck, & Millner, 2016). Connectivity
work has indicated that betweenness and closeness are often not reliably invariance tests if the sum of all absolute edges (i.e., global strength)
estimated (Epskamp, Borsboom, & Fried, 2018); this also occurred in between the two networks differ whereas the network structure
our analyses (see Supplemental Material). Thus, we focus on expected invariance investigates if the two graphs differ statistically.
influence in this manuscript to interpret centrality. Higher expected
influence values suggest that nodes are more central within the network. 2.4.5. Power analysis
We estimated the variance of each node explained by its neighbors (i.e., We used a post-hoc sensitivity analysis to determine if the NP sample
node predictability; Haslbeck & Fried, 2017) using the mgm package was adequate for assessing similarities and differences between both
(Haslbeck & Waldorp, 2015). The predictability of a node is visualized networks. To do this, we simulated datasets with different sample sizes
as a pie chart in the circles surrounding the nodes, with the colored area (i.e., 100, 200, 300, 450, 750, 1000) based on the parameters of the DP
in the outer ring representing the percentage of variance of the node that data set. We used three indices to determine an adequate sample size: 1)
is explained by neighboring nodes. Lastly, the network approach is ideal the correlation between the estimated network and the true network; 2)
for locating symptoms that serve as bridges between symptoms (Cramer, sensitivity – the ability for the estimated network to discover edges; and
Waldorp, Van Der Maas, & Borsboom, 2010). Thus, we also calculated 3) specificity – the extent to which the estimated network can discover
the bridge expected influence values (Jones, Ma, & McNally, 2019) to absent edges. Lastly, we investigated how well expected influence is
detect the sum of all edges between physical panic symptoms and obtained. The simulation study (see Supplemental Material) indicated
cognitive panic symptoms. that 100 participants was an adequate sample size with correlation
values of.85 (N = 200 resulted estimated at.9), a sensitivity value of.78
2.4.3. Network stability (N = 200 resulted estimated at.85), and expected influence of.88 (N =
To test the accuracy and stability of the networks we adhered to the 200 resulted estimated at.94). As expected, the specificity (0.65) did not
guidelines provided by Epskamp et al. (2018) using the bootnet package differ after increasing the sample size due to regularization techniques
(Epskamp, 2015). Stability estimates have only recently been introduced sacrificing specificity for sensitivity (Epskamp & Fried, 2018).
(Epskamp et al., 2018) and at present have not been available for jointly
estimated networks; thus, we examined stability for the two individual 2.4.6. Symptom severity comparisons
networks. First, we used 1000 non-parametric bootstrapping iterations Independent sample two-tailed t-tests were used to examine the
to estimate the accuracy (95% confidence intervals [CI]) of the edge differences in symptom severity ratings between the NP and DP groups.
weights to investigate the accuracy of edges within each network (rec­ Symptom severity ratings were averaged across all 14 symptoms
ommended for ordinal data; see Epskamp et al., 2018) and plotted sig­ (overall), 10 physical symptoms, and 4 cognitive symptoms. Compari­
nificant differences between edge weights. Because regularization is sons for overall symptom severity, physical symptom severity, and
used to estimate the networks, edge-estimates are biased towards zero cognitive symptom severity were examined. Paired sample two-tailed t-
and sampling distributions are not CIs that are centered on the true tests were used to examine differences in overall, physical, and cognitive
parameter value. Importantly, although quantiles overlapping with zero symptom severity for daytime and nocturnal panic attacks reported by
could indicate that the corresponding CI does not overlap with zero, if individuals from the NP group who reported a history of both types of
there is no overlap, then it is known that the corresponding CI does not panic attacks (N = 95). We used the false discovery rate control method
overlap with zero. As such, bootstrapped results should not be used for described by Glickman, Rao, and Schultz (2014) for these four com­
testing if edges are significantly differently from zero (Epskamp et al., parisons to minimize type I error. We included follow-up testing pro­
2018; Fried et al., 2020). Therefore, edge-weight boostrapped CIs should cedures for non-significant results.
only be used to show the accuracy of edge-weight estimates and We used the two one-sided t-test (TOST) approach for equivalence
compare edges to one another, with wider boostrapped CIs indicating testing (Lakens, 2017; Rogers, Howard, & Vessey, 1993; Schuirmann,
that edge strength may be more difficult to interpret (Epskamp et al., 1987) using selected upper and lower limit bounds (90% confidence

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N.S. Smith et al. Journal of Anxiety Disorders 85 (2022) 102514

intervals) based on effect size. With this approach, the null hypothesis is Node predictability (the amount of explained variance of each symptom
that the symptom severity ratings are significantly different at the upper by all other symptoms) is represented by the shaded area surrounding
and lower bounds, and the alternative hypothesis is that both the upper the node. In the DP network panic symptoms explained a mean variance
and lower bounds of the confidence interval are within the bound of of 44.2% and in NP explained a mean variance of 43.8%.
equivalence, thereby rendering the severity ratings between groups The DP and NP networks were strongly correlated with one another
statistically equivalent and clinically unimportant. A sensitivity analysis (r = 0.81). In the DP network, however, the cognitive symptoms were
was conducted using G*Power (v. 3.1) to determine the equivalence more strongly associated with the physical symptoms than in the NP
margin (δ) given the assumption that the true effect is zero, with alpha network, with differences in partial correlation coefficients ranging
level = 0.05, power = 0.80, and sample size of 215, resulting in a from.01 [feeling unreal with fear of going crazy] to.12 [feeling unreal
minimum effect size of d= 0.34. TOST was performed using R (version with fear of losing control], though these differences were not statisti­
4.0.3; R Core Team, 2020) using the “TOSTER” package (Lakens, 2017). cally significant. The strengths of these relationships are depicted in the
When interpreting equivalence testing, if the Null Hypothesis Signifi­ boldness of the lines connecting symptoms in Fig. 1. Inspecting the
cance Test (NHST) is non-significant and the TOST is significant, then graphs, fear of losing control was associated with trembling in the DP
the effect is considered to be statistically equivalent to zero (Lakens, network – as indicated by edge thickness – but appeared less associated
2017). in the NP network. Additionally, detached or unreal feelings was asso­
ciated with hot flashes or cold chills in the DP network, but no such
3. Results association was observed in the NP network.
Interrelationships between physical symptoms were stronger in the
Each group’s data set had less than 1% data missing. Missing data DP network than the NP network as well. For example, racing heart was
were handled by multiple imputation in R using the “MICE” package (v. strongly associated with shortness of breath, moderately associated with
3.8; (Van Buuren and Groothuis-Oudshoorn, 2010)). The MICE package trembling, and very weakly associated with sweating in the NP network.
uses a Fully Conditional Specification algorithm (Buuren & In the DP network, however, racing heart was also moderately associ­
Groothuis-Oudshoorn, 2010), where each continuous variable has its ated with tight or painful chest and weakly associated with hot flashes or
own imputation model using predictive mean matching. Because of the cold chills, nausea, and dizziness. Associations between trembling and
low proportion of missing data (total missing data = 1.1%), a total of choking sensations as well as between hot flashes or cold chills and
five imputations were performed (Enders, 2010; Graham, Olchowski, & numbness were present only in the DP network. Generally, the DP
Gilreath, 2007), resulting in complete data for the network analyses.” network consisted of stronger and more numerous associations between
symptoms compared to the NP network.
Finally, fear of losing control and fear of going crazy were strongly
3.1. Network estimation associated with one another in both networks. The strong association
between these symptoms is unsurprising, given that they are classified as
Descriptive statistics of symptom severity ratings can be found in one symptom in the DSM-5 (APA, 2013). Fear of losing control was
Table 2. Correlations between study variables can be found in Table 3. separated from fear of going crazy in the original Nocturnal Panic Screen
The FGL for DP and NP is presented in Fig. 1 and depicts two clusters of (Craske & Tsao, 2005) because fear of loss of control was thought to
nodes: (1) Physical symptoms of panic disorder; (2) Cognitive symptoms refer specifically to acting in an uncontrolled way whereas fear of going
of panic disorder. The physical symptom cluster contained shortness of crazy was thought to refer to a lack of control over one’s thoughts. Early
breath (“Breath”), pounding heart (“Heart”), chest pain/discomfort nocturnal panic literature sought to differentiate fear of losing control
(“Chest”), feeling dizzy (“Dizzy”), trembling/shaking (“Tremb”), from fear of loss of vigilance, the latter of which was hypothesized to be
sweating (“Sweat”), feelings of choking (“Choke”), chills/heat sensa­ uniquely related to nocturnal panic (Tsao & Craske, 2003).
tions (“HotCold”), nausea/abdominal distress (“Nausea”), and pares­
thesias (“Numb”). The cognitive symptom cluster consisted of 3.2. Network inference
derealization/depersonalization (“Unreal”), fear of losing control
(“Control”), fear of going crazy (“Crazy”), and fear of dying (“Dying”). Next we examined the expected influence and bridge expectance
values between the two networks. The five nodes that exhibited the
Table 2 greatest node expected influence (see Fig. 2) in the DP network were (in
Means and standard deviations for panic symptom severity ratings by group. order) fear of losing control, trembling/shaking, fear of going crazy,
Nocturnal Panic Mean (SD) Daytime Panic Mean (SD) pounding heart, and depersonalization/derealization. Whereas in the
NP network the nodes displaying the greatest expected influence were
1. Breath 2.33 (1.18) 2.39 (1.15)
2. Heart 2.89 (0.89) 2.93 (0.89)
(in order) fear of going crazy, chest pain/discomfort, shortness of
3. Chest 2.15 (1.27) 2.10 (1.35) breath, paresthesias, and feelings of choking.
4. Dizzy 1.74 (1.25) 2.10 (1.35) The highest bridge expected influence values (see Fig. 3) for the DP
5. Tremb 2.37 (1.15) 2.24 (1.24) network were depersonalization/derealization, fear of losing control,
6. Sweat 2.58 (1.22) 1.94 (1.35)
hot/cold sensations, trembling/shaking, and fear of going crazy. For the
7. Choke 1.26 (1.42) .87 (1.21)
8. HotCold 1.96 (1.29) 1.46 (1.26) NP network, the five nodes displaying the largest bridge expected in­
9. Nausea 1.43 (1.35) 1.49 (1.30) fluence were paresthesias, fear of going crazy, fear of losing control,
10. Numb 1.44 (1.28) 1.26 (1.34) depersonalization/derealization, and fear of dying.
11. Unreal 2.43 (1.24) 2.00 (1.38)
12. Crazy 1.91 (1.34) 1.55 (1.44)
13. Control 1.96 (1.35) 2.04 (1.49)
3.3. Network stability
14. Dying 2.04 (1.46) 1.15 (1.41)
Results from the stability analyses suggested that the networks were
Note. Nocturnal Panic N = 107. Daytime Panic N = 108. Symptoms: shortness of
fairly accurately estimated as evidenced by the bootstrapped confidence
breath or smothering sensations (Breath), pounding or racing heart (Heart),
tight or painful chest (Chest), dizziness unsteadiness or faintness (Dizzy), intervals surrounding the edge weights (see Supplemental Material) and
trembling or shaking (Tremb), sweating (Sweat), choking sensations (Choke), adequate edge correlation-stability coefficients (0.28–0.36). The
hot flashes or cold chills (HotCold), nausea or abdominal distress (Nausea), correlation-stability coefficient for expected influence was.29 for DP
numbness or tingling (Numb), detached or unreal feelings (Unreal), fears or and.28 for NP, indicating adequate stability. The correlation-stability
going crazy (Crazy), fears of losing control (Control), fears of dying (Dying). coefficient for bridge expected influence for DP was.29, but.21 for NP.

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N.S. Smith et al. Journal of Anxiety Disorders 85 (2022) 102514

Table 3
Intercorrelations for panic symptom severity ratings.
Mean SD 1 2 3 4 5 6 7 8 9 10 11 12 13

1. Breath 2.36 1.16 –


2. Heart 2.91 .89 .57** –
3. Chest 2.13 1.31 .55** .43** –
4. Dizzy 1.92 1.31 .35** .30** .42** –
5. Tremb 2.31 1.91 .43** .48** .36** .38** –
6. Sweat 2.26 1.32 27** 29** .29** .21** .47** –
7. Choke 1.07 1.33 .33** .12 .42** .43** .29** .23** –
8. HotCold 1.71 1.30 .26** .24** .29** .33** .33** .44** .34** –
9. Nausea 1.46 1.32 .21** .18** .27** .32** .31** .26** .38** .39** –
10. Numb 1.35 1.31 .30** .22** .38** .45** .34** .21** .41** .34** .36** –
11. Unreal 2.21 1.33 .30** .24** .30** .34** .33** .13 .35** .35** .14* .40** –
12. Crazy 1.73 1.40 .38** .23** .38** .34** .36** .24** .33** .40** .30** .42** .54** –
13. Control 2.00 1.42 .39** .27** .40** .40** .40** .20** .33** .25** .23** .28** .50** .74** –
14. Dying 1.59 1.50 .26** .16* .28** .27** .26** .19** .27** .30** .14* .35** .45** .56** .48**

Note. **p < .01. *p < .05. Symptoms: shortness of breath or smothering sensations (Breath), pounding or racing heart (Heart), tight or painful chest (Chest), dizziness
unsteadiness or faintness (Dizzy), trembling or shaking (Tremb), sweating (Sweat), choking sensations (Choke), hot flashes or cold chills (HotCold), nausea or
abdominal distress (Nausea), numbness or tingling (Numb), detached or unreal feelings (Unreal), fears or going crazy (Crazy), fears of losing control (Control), fears of
dying (Dying).

the global strength test (S=0.03, p = .98) or centrality test (C=− 0.15,
p = .25). These results indicate that the two networks are not statisti­
cally different.

3.5. Symptom severity comparisons

3.5.1. Overall symptom severity between groups


An independent sample two-tailed t-test between the DP and NP
group overall symptom severity mean rating revealed a statistically
significant difference, t(213) = − 2.025, p = .04. After accounting for
false discovery rates, however, this result no longer reached the signif­
icance threshold. To test if this lack of a significant difference was
clinically unimportant, we conducted an equivalence test (TOST). The
equivalence test was not significant, t(213) = 0.758, p = .23, indicating
that the difference in overall symptom severity ratings between the NP
and DP groups was not statistically equivalent. The NP group rated
symptom severity at 2.04 on average whereas the DP group rated
symptom severity at 1.82 on average. This non-significant difference
indicates that the NP group experienced panic symptoms as somewhat
more intense than the DP group, but the difference may be unreliable.

3.5.2. Overall symptom severity within nocturnal panic group


A paired sample two-tailed t-test between the daytime and nocturnal
Fig. 1. Visualization of Fused Graphical Lasso (FGL) estimated networks of panic attack overall symptom severity ratings for individuals who re­
daytime panic (left) and nocturnal panic (right). Each node represents a
ported a history of both types of panic attacks (N = 95) revealed a sta­
symptom. Each edge represents the regularized partial correlation between
tistically significant difference, t(94) = 3.012, p = .003. This result
symptoms. Edge thickness illustrates the degree of positive association. The
shaded gray rings around the nodes represent the predictability (i.e., variance remained significant after accounting for false discovery rates. This
of a node explained by all its neighbors). “Chs” = chest pain/discomfort; “Brt” subsection of the NP group rated nocturnal panic symptom severity at
= shortness of breath; “Hrt” = pounding heart; “Trm” = trembling/shaking; 2.09 on average and daytime panic symptom severity at 2.24 on
“Swt” = sweating; “HtC” = chills/heat sensations; “Nas” = nausea/abdominal average. Thus, the NP group rated panic attacks out of a wakeful state as
distress; “Chk” = feelings of choking; “Dzz” = feeling dizzy; “Nmb” more severe than panic attacks out of a sleeping state.
= paresthesias; “Cnt” = fear of losing control; “Crz” = fear of going crazy;
“Unr” = derealization/depersonalization; and “Dyn” = fear of dying. 3.5.3. Physical symptom severity between groups
An independent sample two-tailed t-test between the DP and NP
This indicates that bridge expected influence values may be unreliable in group physical symptom severity mean ratings revealed no statistically
the current sample. Overall, these stability estimates are on the low end significant difference, t(213) = − 1.616, p = .11. To test if this lack of a
of acceptability (>0.25; Epskamp et al., 2018) and should be interpreted significant difference was clinically unimportant, we conducted an
with caution. equivalence test (TOST). The equivalence test was not significant, t
(213) = − 0.005, p = .50, indicating that the difference between phys­
ical symptom severity ratings is not statistically equivalent. These results
3.4. Network comparison indicate that the differences found in physical symptom severity ratings
between DP and NP groups can neither be considered statistically
Correlations between the adjacency matrices (r = 0.64), predict­ different nor equivalent.
ability nodes (r = 0.33), and centrality indices (r = 0.31) for the two
networks suggested weakly to moderately similarity across groups. The
network invariance test was not significant (M=0.23, p = .86), nor was

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N.S. Smith et al. Journal of Anxiety Disorders 85 (2022) 102514

Fig. 2. Expected influence values for each node


in the Daytime (blue) and Nocturnal panic (red)
networks. Nodes with greater influence are
more central to the network. “1-Brth”
= shortness of breath; “2-Hrt” = pounding
heart; “3-Chst” = chest pain/discomfort; “4-
Dzzy” = feeling dizzy; “5-Trmb” = trembling/
shaking; “6-Swt” = sweating; “7-Chke”
= feeling of choking; “8-HtC” = chills/heat
sensations; “9-Nsea” = nausea/abdominal
distress; “10-Numb” = paresthesias; “11-Unrl”
= depersonalization/derealization; “12-Crzy”
= fear of going crazy; “13-Cont” = fear of
losing control; “14-Dyng” = fear of dying.

3.5.4. Cognitive symptom severity between groups associative patterns between symptoms or identify if patterns differ
An independent sample two-tailed t-test between the DP and NP based on the state the individual is in when the panic occurs (i.e.,
group cognitive symptom severity mean ratings revealed a statistically sleeping, awake). Our hypotheses were largely unsupported. Overall,
significant difference, t(213) = − 2.394, p = .02. This result remained the network structures of NP and DP groups were largely similar,
significant after accounting for false discovery rates. The NP group rated although the number and strengths of associations between symptoms
cognitive symptom severity at 1.97 on average whereas the DP group differed between networks. Panic severity ratings were also not statis­
rated cognitive symptom severity at 1.57 on average. This small but tically equivalent between panic groups, types of panic attacks, or types
significant difference indicates that despite the fact that nocturnal panic of panic symptoms. Interestingly, individuals in the NP group rated
occurs out of a sleeping state with no cognitive triggers, the NP group panic attacks that they experienced while awake as more severe than
still experienced cognitive symptoms as somewhat more intense than those experienced out of a sleeping state. The NP group also rated
the DP group. cognitive symptoms as more severe than the DP group, despite nocturnal
panic being described by Craske and Rowe (1997) as “purely biological”.
4. Discussion Prior research has suggested that because nocturnal panic onset occurs
in the absence of cognitive processes or triggering behavioral events, it
The present study directly compared the associations between cannot be caused by catastrophic cognitions (Craske & Rowe, 1997;
nocturnal and daytime panic attack symptoms using a network analysis Labbate et al., 1994). Thus, catastrophic cognitions occurring during
approach. This is the first study, to our knowledge, to use network nocturnal panic, presumably after the individual wakes due to the
analysis to examine the interrelationships between reported panic attack physical symptoms, have been largely ignored. The results of the present
symptoms. Panic symptoms have long been theorized to perpetuate one study suggest that although cognitive symptoms may not cause
another in a forward feedback loop (Schmidt et al., 1997; Uhde, 1994); nocturnal panic attack onset, they do contribute to distress and likely
however, no study has used network analysis to identify specific play a role in perpetuating physical symptoms after the individual

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N.S. Smith et al. Journal of Anxiety Disorders 85 (2022) 102514

Fig. 3. Bridge expected influence values for


each node in the Daytime (blue) and Nocturnal
panic (red) networks. Nodes with greater bridge
expected influence may be most influential for
functioning as a bridge between physical and
cognitive panic symptoms. “1-Brth” = shortness
of breath; “2-Hrt” = pounding heart; “3-Chst”
= chest pain/discomfort; “4-Dzzy” = feeling
dizzy; “5-Trmb” = trembling/shaking; “6-Swt”
= sweating; “7-Chke” = feeling of choking; “8-
HtC” = chills/heat sensations; “9-Nsea”
= nausea/abdominal distress; “10-Numb”
= paresthesias; “11-Unrl” = depersonalization/
derealization; “12-Crzy” = fear of going crazy;
“13-Cont” = fear of losing control; “14-Dyng”
= fear of dying.

awakens. The maintaining role of cognitive symptoms in nocturnal information about the order in which symptoms occur; thus, future
panic may help to account for the efficacy of Cognitive Behavioral longitudinal studies are required to determine when cognitive symp­
Therapy (CBT) approaches to treatment (Craske, Lang, Aikins, & Myst­ toms begin in daytime compared to nocturnal panic attacks.
kowsk, 2005). Individuals in the NP group rated panic symptoms as somewhat more
Daytime and nocturnal panic network structures were not statisti­ severe than the DP group despite prior literature demonstrating that
cally different, indicating that the interrelationships between panic nocturnal panic does not constitute a more severe form of panic disorder
symptoms are largely similar regardless of whether the panic begins (Craske et al., 2002). Craske and colleagues (2002), however, found a
while the individual is awake or asleep. Several more subtle differences lack of difference between symptoms characteristic of the disorder (e.g.,
in symptom associations were noted, however, which provide directions agoraphobic avoidance, interpersonal functioning impairment) rather
for future research. First, although cognitive symptoms were not more than differences in the experience of the panic attacks themselves. In
central to the DP network, they did produce more relationships with contrast to the Craske et al. (2002) study, the current study was not
physical symptoms compared to the NP network. Those cognitive- limited to individuals who met criteria for panic disorder, but included
physical symptom relationships were also stronger in the DP versus participants who had experienced panic attacks regardless of psycho­
NP networks. It is possible that cognitive symptoms are more inter­ logical diagnoses. Therefore, it is possible that individuals who panic out
connected in the DP network because they are present throughout the of sleep do experience more severe panic attacks without also experi­
panic experience when panic originates from a wakeful state. encing more fear of future panic attacks, avoidance behaviors, and
Conversely, in nocturnal panic, panic symptoms begin during non-REM functional impairment. Differences in reported severity related to ex­
sleep, when there is no opportunity for cognitive activity (Craske & pected versus unexpected daytime panic may also be relevant. The
Rowe, 1997). Thus, cognitive panic symptoms can only occur after the current study did not separate daytime panic symptom ratings based on
individual wakes up, already experiencing a constellation of physical whether or not the individual was aware of external factors leading to
panic symptoms. Importantly, cross-sectional analyses cannot provide the panic attack. Previous literature has indicated that expected panic

8
N.S. Smith et al. Journal of Anxiety Disorders 85 (2022) 102514

attacks are rated as less severe than unexpected daytime panic attacks ratings, particularly the more severe cognitive symptom ratings reported
(Brown et al., 2016). Thus, future studies should separate daytime panic by the nocturnal panic group provide new insights and challenge pre­
severity ratings based on whether they were expected or unexpected to vious conceptualizations of nocturnal panic as a purely biological form
clarify this point. It is possible that nocturnal panic attacks are rated of panic. Future research is needed to clarify the role of cognitive
equally severe compared to unexpected daytime panic, but more severe symptoms in nocturnal panic.
than expected daytime panic. Accounting for the nature of daytime
panic severity may also help to clarify the severity ratings of physical Acknowledgments
symptoms, which were neither statistically different nor equivalent in
the current study. None.
Cognitive symptoms were rated as significantly more severe in This research did not receive any specific grant from funding
nocturnal compared to daytime panic attacks. This finding did not agencies in the public, commercial, or not-for-profit sectors.
support our hypothesis and challenges the conceptualization of
nocturnal panic as a purely biological event (Labbate et al., 1994; Sha­ Declarations of interest
piro & Sloan, 1998). Given that nocturnal panic begins during the
transition between Stage II and Stage III sleep, during which there are no none.
dreams or nightmares (Craske & Rowe, 1997), it is possible that
cognitive symptoms play no role in initiating the panic episode but occur Appendix A. Supporting information
when the individual is awakened. This may also help to explain the lack
of associations between cognitive and physical symptoms in the Supplementary data associated with this article can be found in the
nocturnal panic symptom network. Physical symptoms may develop online version at doi:10.1016/j.janxdis.2021.102514.
first, while the individual is still sleeping, then intensify to the point of
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