Gender Differences in Neurocognitive ... - Wiley Online Library

Journal of Traumatic Stress February 2018, 31, 64–70

Gender Differences in Neurocognitive Performance Among Children With Posttraumatic Stress Disorder and Mild Traumatic Brain Injury Shira Segev,1,2 Maayan Shorer,2 Tammy Pilowsky Peleg,5,6 Alan Apter,2 Silvana Fennig,2 and Yuri Rassovsky1,3,4 1

Department of Psychology, Bar Ilan University, Ramat-Gan, Israel PTSD Unit, Department of Psychological Medicine, Schneider Children’s Medical Center of Israel, Petach Tikvah, Israel 3 Leslie and Susan Gonda (Goldschmied) Multidisciplinary Brain Research Center, Bar Ilan University, Ramat-Gan, Israel 4 Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles (UCLA), California, USA 5 Neuropsychological Unit, Schneider Children’s Medical Center of Israel, Petach Tikvah, Israel 6 Department of Psychology, The Hebrew University of Jerusalem, Jerusalem, Israel

2

Posttraumatic stress disorder (PTSD) and mild traumatic brain injury (mTBI) are frequent sequelae after motor vehicle accidents (MVAs). These two pathologies often have overlapping neurocognitive deficits across several domains, such as attention, memory, and executive functions. The present study was an effort to examine the contribution of gender to these overlapping symptoms. To this end, psychodiagnostic and neuropsychological data were collected on 61 children and adolescents 3 months following MVA. All participants were diagnosed with PTSD, and about half (n = 33) also received a diagnosis of mTBI. Analyses of variance revealed significant interactions between gender and mTBI (η2p = .15), such that girls with mTBIs preformed significantly worse than noninjured girls on measures of executive functions (Cohen’s d = 3.88) and sustained attention (Cohen’s d = 3.24). Boys, on the other hand, did not differ significantly on any of those measures, irrespective of TBI injury status. Similarly, comparisons to the normative population revealed that, whereas boys showed impaired neurocognitive performances regardless of TBI status, impaired performances in girls were limited to those cases in which the girls were comorbid for PTSD and mTBI. It appears then that whereas PTSD alone might explain boys’ reduced neurocognitive performance, among girls the comorbidity of PTSD and mTBI is required to account for performance deficits.

Motor vehicle accidents (MVAs) are one of the leading causes of the development of posttraumatic stress disorder (PTSD), as well as for mild traumatic brain injury (mTBI), in childhood (Berrigan, 2012; Marshall et al., 1999; McKinlay et al., 2008). Both conditions often occur following a traumatic event and share many sequelae, including irritability, insomnia, restlessness, depression, and anxiety (Kennedy et al., 2007; Sbordone & Ruff, 2010). Moreover, impaired neurocognitive functioning, such as weakened memory, executive function, and attention deficits, are common with both mTBI (Catale, Marique, Closset, & Meulemans, 2009; Scherwath et al., 2011) and PTSD (Beers & De Bellis, 2002; Sbordone & Ruff, 2010).

Despite symptom overlap, recovery courses differ substantially for these conditions (Vasterling, Verfaellie, & Sullivan, 2009). Whereas impaired neurocognitive functioning associated with mTBIs may resolve within several weeks to several months postinjury (Carroll et al., 2004), neurocognitive deficits associated with PTSD may persist for many years after exposure to trauma (Turley & Obrzut, 2012). Recovery outcome may be further affected when mTBI and PTSD co-occur. Findings regarding cumulative deficits of mTBI and PTSD are conflicting. A number of studies that have examined combat veterans found no differences in neurocognitive performance between noncomorbid and comorbid samples of mTBI with PTSD (Brenner et al., 2009; Gordon, Fitzpatrick, & Hilsabeck, 2011). Conversely, more recent research by Combs et al. (2015) found greater neurocognitive impairment (e.g., deficits in visual scanning, attention, and psychomotor speed, and delayed verbal memory) among veterans with comorbid mTBI and PTSD than among veterans with PTSD or mTBI alone (although both samples included participants who suffered from multiple mTBIs, which may account for some of the differences). Pineau,

This study was carried out as part of a PhD dissertation by Shira Segev at Bar Ilan University, Ramat Gan, Israel. This study was supported in part by a grant from the Israel Insurance Association. Correspondence concerning this article should be addressed to Prof. Yuri Rassovsky, Department of Psychology, Bar-Ilan University, Ramat-Gan 52900 Israel. Email: [email protected] C 2018 International Society for Traumatic Stress Studies. View Copyright this article online at wileyonlinelibrary.com DOI: 10.1002/jts.22250

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Comorbidity and Neurocognitive Gender Differences

Marchand, and Guay (2014) also found greater deficiency in long-term verbal memory among individuals with comorbidity of PTSD and mTBI in comparison to those with PTSD or TBI alone. The few studies available in this area suggest then that mTBI and PTSD may cumulatively and/or differentially impact neuropsychological and emotional functioning. The potentially differential sequelae following mTBI and PTSD has received even less attention in pediatric populations. It is reasonable to assume that in children, the impact of traumatic injury would display an even more divergent pattern, as it occurs during a critical period of brain development. In our previous study, we found that children with both PTSD and mTBI following MVA did not differ from children diagnosed with PTSD alone in their neurocognitive performance (Segev et al., 2016). However, in light of the conflicting findings in the literature, it is necessary to investigate this issue further by taking into account relevant moderating factors. A potential moderating variable that may partly explain these conflicting findings is gender, which unfortunately is often overlooked in studies examining mTBI and/or PTSD. Despite the paucity of studies that have investigated gender differences in neurocognitive performance among individuals diagnosed with PTSD, there is some evidence that has suggested that male gender may be related to a more severe neurocognitive dysfunction. For example, Scott et al. (2015) conducted a broad meta-analysis that investigated the differences in neurocognitive performance between individuals with PTSD and healthy control groups. They found that as the percentage of men in the sample increased, so did the magnitude of the effect size estimate (i.e., the difference between the groups), indicating a greater performance discrepancy between the PTSD and the control groups. Another set of studies has suggested that female gender may be associated with greater concussion-related dysfunction. For example, several studies have shown that female high school and college athletes not only exhibit a greater likelihood of cognitive impairment following a concussion than their male counterparts, but also demonstrate greater severity of neurocognitive impairment, including poorer visual memory performance, slower reaction times, and reduced processing speed (Broshek et al., 2005; Covassin, Elbin, Harris, Parker, & Kontos, 2012). Moreover, girls tend to report more concussive symptoms and may take longer to recover from a concussion than boys (Blinman, Houseknecht, Snyder, Wiebe, & Nance, 2009; Colvin et al., 2009). As far as we have been able to ascertain, no studies to date have addressed gender differences in neurocognitive performance among children diagnosed with PTSD and mTBI. Even the aforementioned findings that addressed gender differences in the effect of mTBI on cognition focused only on the acute postinjury phase and did not take into consideration the impact of emotional trauma. The present study thus examined the differential effect of gender on belated neurocognitive performances in children diagnosed with PTSD with or without mTBI.

Method Participants and Procedure A total of 61 children and adolescents (n = 38 boys) were recruited from the Posttraumatic Stress Disorder Clinic at the Schneider Children’s Medical Center. The current study was embedded within a larger project that examined treatment efficacy among MVA survivor diagnosis with PTSD and mTBI, and the sample is described in detail elsewhere (Segev et al., 2016). Participants’ ages ranged from 6 to 18 years (M = 11.9, SD = 3.16), and they were evaluated at least 3 months following the MVA (M = 16.95, SD = 16.2). Table 1 summarizes key demographic and clinical characteristics for boys and girls. No differences were found on background variables, psychiatric diagnoses, emotional status, and intellectual functioning. The only significant difference was a higher frequency of constant pharmaceutical care among boys. However, attention deficit/hyperactivity disorder (ADHD) and/or other psychiatric diagnoses were similar in both groups and cannot explain this discrepancy. Power analysis with a medium effect size of ƒ2 = 0.2, at alpha of .05 and 61 participants, yielded an adequate power of 0.97 for our analyses. All participants met Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.; DSM-IV-TR; American Psychiatric Association [APA], 2000) criteria for PTSD. The study was approved by the Institutional Review Boards at Bar-Ilan University and the Schneider Children’s Medical Center of Israel, and all participants and their parents gave written informed consent for participation. During the initial assessment, participants and their parents met with a psychologist for an evaluation of mental status, injury characteristics, and diagnosis of PTSD. The Kaufman Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (KSADS-PL; Kaufman et al., 1997) was administered separately to both parents and child. Each child also completed self-report questionnaires regarding their PTSD symptoms (Child PTSD Symptoms Scale; Foa, Johnson, Feeny, & Treadwell, 2001) as well as an adaptation of the Post-Concussive Symptom Interview (PPCS; Mittenberg, Wittner, & Miller, 1997). Diagnosis of mTBI (n = 33) was based on information from each participant’s medical records, using standard criteria (American Congress of Rehabilitation Medicine, 1993). Further assessments were conducted at the Neuropsychological Unit, where participants completed a standardized neuropsychological evaluation, administered by a trained clinician blind to each participant’s psychological state and medical history (including the presence or absence of mTBI). Measures Data concerning injury characteristics were collected from each child’s medical records. The status of mTBI was established by a senior clinician. Demographic information (time since the accident, socioeconomic status, family status, ethnicity, psychiatric or medical background, and status of litigation

Journal of Traumatic Stress DOI 10.1002/jts. Published on behalf of the International Society for Traumatic Stress Studies.

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Table 1 Demographic Information and Psychiatric, Emotional, and Intellectual Status for Boys and Girls Group

Variable TBI Age, years Hebrew Married parents Income Months since the accident Litigation Psychiatric symptoms PPCS Global scale a No additional psychiatric diagnosis ADHD diagnosis Constant pharmaceutical care PTSD symptomsb Depression symptoms c State anxiety d Parental PTSD symptoms Nonverbal intelligence

Boys

Girls

(n = 38)

(n = 23)

n

%

21

55.3

19 28

M

SD

11.63

3.04

50.0 73.7

12

52.2

0.52 0.36 0.42 0.66 28.23

T

12.44

3.48

−0.95

χ2

P

0.06

.814 .344 .246 .716 .297 .175 .201

1.34 0.67 0.80 11.17

−1.05 1.37

87.0

0.22 12.19

1.63 0.67 62.31

19 5 2 1.63 0.65 1.88 1.36 29.44

SD

2.56 13.30 20

71.1 23.7 31.6

M

65.2 78.3

0.67 18.49

73.0 0.59 59.54

27 9 12

%

15 18 2.36 19.16

27

n

0.20 12.08

−1.39 −0.86

82.6 21.7 8.7

1.03 0.03 4.24 1.74 0.71 2.05 1.43 40.18

0.49 0.40 0.50 0.93 34.37

−0.82 −.65 −1.43 −0.37 −1.33

.169 .392 .310 .861 .039* .419 .520 .157 .712 .190

Note. TBI = traumatic brain injury; PPCS = Postconcussion Symptoms Inventory (PCS-I); ADHD = attention deficit/hyperactivity disorder; PTSD = posttraumatic stress disorder. a Measured using the Children’s Global Assessment Scale (CGAS). b Measured using the Child Posttraumatic Stress Disorder Symptoms Scale (CPSS). c Measured using the Children Depression Inventory (CDI). d Measured using the State-Trait Anxiety Inventory for Children (STAI-C). e Measured using the Raven’s Progressive Matrices (RPM). *p < .05.

procedures related to the accident) was collected through structured interviews given by the clinician. Effort and motivation were evaluated using the Test of Memory Malingering (TOMM), a standardized symptom validity test (Tombaugh, 1996), which has been repeatedly examined in the pediatric population (Blaskewitz, Merten, & Kathmann, 2008). Executive function performance was evaluated using the sorting, design fluency, and trail-making subtests from the Delis-Kaplan Executive Function System (D-KEFS; Delis, Kaplan, & Kramer, 2001), the Digit Span subtest (WISC-IV HEB; PsychTech LLC, 2010), and the Spatial Span subtest (WISC-IV Integrated; Kaplan, Fein, Kramer, Delis, & Morris, 2004). Sustained and focused attention were assessed using the commissions and omissions subscales of Conners’ Continuous Performance Test II-Version 5 (CPT II V. 5; Conners, 2004). Subtest mean scores were used to calculate the score for each domain. Data Analysis We used TOMM recommended cut-off score (< 45) to exclude participants who demonstrated suboptimal effort

and motivation (Tombaugh, 1996). Based on this criterion, eight participants (six with mTBI and two without mTBI) were excluded from subsequent analyses. To examine group differences in mean scores on neurocognitive variables, we conducted a two-way multivariate analyses of variance (MANOVA) with gender and TBI (mTBI vs. non-TBI) as between-subjects independent variables, with executive functions and sustained attention as dependent variables. Although the groups did not significantly differ on time (in months) since the accident, given the substantially differential range of time that had elapsed since the injury between boys and girls, we conducted multivariate analyses of covariance (MANCOVA), with time since the accident as a covariate. As the inclusion of this covariate did not modify any of the multivariate tests or the gender-by-TBI interaction, Wilks’s lambda = .85, F(1, 48) = 4.3, p = .019, η2p = .16, it was excluded from subsequent analyses. Further simple effects were tested using separates ANOVAs. Neurocognitive performance of the current sample was also examined against standardized age norms using one sample t test. There were no univariate or multivariate withincell outliers. Results of evaluation of assumptions of normality,


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Table 2 Clinical and Neurocognitive Differences Between Gender and Traumatic Brain Injury (TBI) Groups Boys

Parameter Age (years) Months since the accident PPCS (z score) PTSD symptoms (z score) Executive functions (z score) Sustained attention (z score) Parameter Premorbid ADHD

Girls

mTBI

Non-mTBI

mTBI

Non-mTBI

(n = 19)

(n = 15)

(n = 8)

(n = 11)

M

SD

M

SD

M

SD

M

SD

F

p

η2p

12.50 20.95 0.57 1.66 −0.58 −0.27 n 5

2.75 21.20 0.26 0.43 0.14 0.20 % 14.7

9.79 18.53 0.56 1.50 −0.54 −0.75 n 4

2.80 17.34 0.17 0.66 0.15 0.23 % 11.8

12.20 14.88 0.56 1.69 −0.57**a −1.18*a n 1

3.88 8.84 0.14 0.41 0.21 0.32 % 5.3

12.52 11.09 0.66 1.67 0.19 −0.23 n 4

3.35 9.27 0.19 0.54 0.18 0.27 % 21.1

2.89 0.02 0.64 0.23 4.31 7.75 χ2 0.00

0.095 0.888 0.427 0.633 0.043 0.008

.06 .00 .01 .01 .08 .14

0.990

.00

Note. mTBI = mild traumatic brain injury; PPCS = postconcussion symptoms inventory; PTSD = posttraumatic stress disorder; ADHD = attention deficit/hyperactivity disorder. a Numbers represent significant differences relative to the noninjured group per gender. *p < .05. **p < .01.

homogeneity of variance-covariance matrices, linearity, and multicollinearity were all within acceptable limits. There were 10 participants from the original sample who dropped out and did not complete the neuropsychological assessment. To address the issue of missing data, the analyses were conducted using two methods: list-wise deletion and maximum-likelihood expectation-maximization. As results using both methods led to the same conclusions, we report here only the results based on maximum-likelihood expectationmaximization (Jamshidian & Bentler, 1999).

As this study did not include an age-matched control sample, the sample’s mean scores were compared to normative values (population mean z score = 0). The t tests showed impaired neurocognitive performance in the sample of boys, regardless of TBI diagnosis (except on sustained attention score among TBI-injured boys). Conversely, the girls’ sample showed a different pattern of findings, such that girls with TBI preformed significantly below the norm, whereas girls with PTSD only (i.e., non-TBI) preformed within their normative range (see Figure 1). Discussion

Results The four groups did not differ on any of the demographic variables, age, premorbid ADHD, PTSD, or PPCS symptom ratings. Descriptive statistics for study groups (TBI by gender) are presented in Table 2. Multivariate analyses were conducted in order to examine the neurocognitive differences between groups. Tests of between subject effects indicated significant group differences in gender, Wilks’s lambda = .86, F(1, 49) = 3.85, p = .028, η2p = .14. A statistically significant multivariate interaction was found between gender and TBI on the subscales, Wilks’s’ lambda = .85, F(1, 49) = 4.31, p = .019, η2p = .15. Separate ANOVAs for each variable revealed that girls with TBI performed significantly worse, Wilks’s lambda = .84, F(1, 49) = 4.5, p = .016 η2p = .16, on measures of executive function, F(1, 49) = 7.53, p = .008, Cohen’s d = 3.88, and sustained attention, F(1, 49) = 5.29, p = .026, d = 3.24, than noninjured girls. In contrast, no significant differences on any of the measures were found between the boys’ subgroups (see Table 2).

The present study was an effort to further understand genderrelated neurocognitive differences among comorbid pediatric patients following MVA. Multivariate analyses revealed a significant interaction between gender and TBI injury. These findings indicate that among children diagnosed with PTSD, a comorbid TBI significantly affects girls’ neurocognitive performance, whereas boys are less affected by TBI. On the other hand, in the present subsample of children diagnosed with PTSD and without a comorbid mTBI, girls functioned cognitively within normative levels, whereas boys performed below normative levels and similar to boys with comorbid PTSD and mTBI. Notably, when evaluated together, gender differences were obscured, such that girls and boys diagnosed with comorbid PTSD and mTBI demonstrated the same patterns of neurocognitive performance. The association between PTSD and persistent neurocognitive deficits is consistent with boys’ reduced neurocognitive performance (Turley & Obrzut, 2012), a deficit that was not evident in girls with PTSD. This finding is compatible with previous


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Figure 1. Neurocognitive performances relative to age norms. All neurocognitive functioning represented in z scores. *p < .05. **p < .01. ***p < .001.

studies that have suggested that cognitive impairments in individuals suffering from PTSD are more pronounced in male than female participants (Scott et al., 2015). These gender differences are substantially understudied in mTBI and PTSD literature and require further attention. The lack of differences between boys suffering from PTSD with and without mTBI also deserves additional investigation. One possible explanation is that because boys suffering from PTSD present greater neurocognitive deficits than girls (Scott et al., 2015) and are less vulnerable than girls to mTBI outcomes (Blinman et al., 2009; Colvin et al., 2009; Covassin et al., 2012; Farace & Alves, 2000), the additive effect of mTBI in boys might have been obscured. However, larger studies would be required to disentangle this intriguing finding. In contrast to the lack of deferential neurocognitive pattern in boys, the girls in our study did demonstrate the additive effect of mTBI and PTSD. In other words, neurocognitive impairments were seen in girls with PTSD only if they also suffered

mTBI. This finding suggests that girls may be vulnerable to the PTSD-mTBI comorbidity. One possible mechanism that may explain this vulnerability among girls relates to premorbid factors. Farace and Alves (2000), for example, claim that the lower incidence of TBI in women compared with men (Kraus & Nourjah, 1988) potentially reflects systematic differences between women who sustain TBI and the general female population (e.g., girls who sustain TBI may have premorbidly poorer executive functions, thereby being at a higher risk for impulsive behavior that leads to accidents, such as getting hit by a car as a pedestrian, or involvement in a car crash without being properly belted). It should be noted that in the present study, the female mTBI group did not have greater prevalence of premorbid ADHD than the non-mTBI female group, but additional research addressing this specific hypothesis is necessary to rule out this potential explanation. It is also possible that the girls’ vulnerability to the comorbidity of PTSD and mTBI is due to posttraumatic alterations in



the normal physiology of gonadal steroids. For example, it was suggested that injury to the anterior pituitary, which produces follicle-stimulating hormone and luteinizing hormone, could disrupt endogenous estrogen and/or progesterone production and reduce the neuroprotective effect of these hormones, or even lead to “withdrawal” in human females of child-bearing age (Bazarian et al., 2009). Indirect support for this hypothesis comes from studies in which post-TBI outcomes in males and females were compared. These studies reported poorer outcomes in females than in males during the postmenarche and premenopause years (Davis et al., 2006; Morisson et al., 2004). As most of the girls in the TBI group in the present study were over 13 years of age (66.0%), this explanation is plausible. Unfortunately, the sample in our study was too small to directly examine age differences among girls. Another intriguing physiological explanation has been suggested by Farace and Alves (2000). They point to a growing body of evidence that demonstrates greater bilateral processing in women than in men. According to these authors, the focal brain organization in men might actually have a protective benefit in cases of TBI. Namely, given the often diffuse nature of TBI, women may be affected to a greater extent than men (Farace & Alves, 2000). The results of this study should be interpreted in light of certain limitations, including the small sample size, high temporal variance since MVA, broad age range of participants, and lack of an age-matched control group. Results are also limited by the cross-sectional design of our study and by a possible selection bias in recruiting families who actively sought treatment. It should be noted that findings did not change when we controlled for effort and so cannot be explained by motivation issues. Taken together, these results underscore the importance of gender differences in neurocognitive deficits among children diagnosed with PTSD and mTBI, assessed several months postinjury, and suggest that these differences should be taken into consideration when conducting research on the neurocognitive sequelae of these disorders, as well as in treatment planning. On a more practical level, these results suggest that boys with noncomorbid PTSD might still require cognitive remediation, whereas such intervention for girls would be necessary only if they also sustained mTBI. Our findings thus support an individual-oriented therapy approach, which includes individual differences, such as gender, as part of treatment planning and implementation.

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