Journal of the International Neuropsychological Society (2020), 1–14

Copyright © INS. Published by Cambridge University Press, 2020.

doi:10.1017/S1355617720000193

Trajectory of 10-Year Neurocognitive Functioning After

Moderate–Severe Traumatic Brain Injury: Early Associations
and Clinical Application

Solrun Sigurdardottir1,* , Nada Andelic2,3, Cecilie Røe2,3,4 and Anne-Kristine Schanke1

1
Department of Research, Sunnaas Rehabilitation Hospital, Nesoddtangen, Norway
2
Department of Physical Medicine and Rehabilitation, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway
3
Institute of Health and Society, Research Centre for Habilitation and Rehabilitation Models and Services (CHARM), Faculty of Medicine, University of Oslo,
Oslo, Norway
4
Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Norway

(RECEIVED March 15, 2019; FINAL REVISION January 10, 2020; ACCEPTED January 16, 2020)

Abstract
Objective: This study aimed to explore the 10-year trajectories of neurocognitive domains after moderate–severe
traumatic brain injury (TBI), to identify factors related to long-term neurocognitive functioning, and to investigate
whether performance remained stable or changed over time. Method: Seventy-nine patients with moderate–severe TBI
between the ages of 16 and 55 years were assessed at 3 months, 1, 5, and 10 years postinjury using neuropsychological
tests and functional outcomes. Three hierarchical linear models were used to investigate the relationships of domain-
specific neurocognitive trajectories (Memory, Executive function, and Reasoning) with injury severity, demographics,
functional outcome at 3 months (Glasgow Outcome Scale-Extended) and emotional distress at 1 year (Symptom
Checklist 90-Revised). Results: Education, injury severity measures, functional outcome, and emotional distress were
significantly associated with both Memory and Executive function. Education and emotional distress were related to
Reasoning. The interaction effects between time and these predictors in predicting neurocognitive trajectories were
nonsignificant. Among patients with data at 1 and 10 year follow-ups (n = 47), 94–96% exhibited stable scores on
Executive function and Reasoning tasks, and 83% demonstrated stable scores on Memory tasks. Significant memory
decline was presented in 11% of patients. Conclusions: The findings highlight the differential contribution of variables
in their relationships with long-term neurocognitive functioning after moderate–severe TBI. Injury severity was
important for Memory outcomes, whereas emotional distress influenced all neurocognitive domains. Reasoning
(intellectual) abilities were relatively robust after TBI. While the majority of patients appeared to be cognitively stable
beyond the first year, a small subset demonstrated a significant memory decline over time.
Keywords: Cognitive impairment, Longitudinal, Recovery, Emotional distress, Rehabilitation, TBI

INTRODUCTION after diffuse axonal injury and contusions, particularly in

the frontal and temporal lobes, which are brain regions impor-
Neurocognitive dysfunction is arguably the most central
tant in Memory and Executive function (Haberg et al., 2015;
characteristic of moderate–severe traumatic brain injury
Wood & Worthington, 2017). In terms of neurocognitive
(TBI), with significant deficits in the acute stage that may per-
recovery after TBI, early spontaneous improvement is typi-
sist many years after injury (Draper & Ponsford, 2008;
cally observed in the initial weeks and months after injury
Himanen et al., 2006; Millis et al., 2001). Long-standing cog-
and maintained throughout the first year (Christensen et al.,
nitive impairments can influence all areas of the individual’s
2008; Finnanger et al., 2013).
life and make participation in work and society challenging
Stability in cognitive recovery is often reached approxi-
(Gautschi et al., 2013; Grauwmeijer et al., 2018; Ponsford,
mately 1–2 years after injury (Rabinowitz, Hart, Whyte, &
Draper, & Schonberger, 2008). These impairments occur
Kim, 2018; Ruttan, Martin, Liu, Colella, & Green, 2008).
However, a complete recovery is unlikely, and individuals
*Correspondence and reprint requests to: S. Sigurdardottir, PhD,
Department of Research, Sunnaas Rehabilitation Hospital, Bjørnemyrveien with moderate–severe TBI continue to exhibit cognitive dif-
11, Nesoddtangen 1450, Norway. Email: sosigu@ous-hf.no ficulties 5 and 10 years after injury (Hetherington, Stuss, &
1
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 2 S. Sigurdardottir et al.
Finlayson, 1996; Marsh, Ludbrook, & Gaffaney, 2016), with
larger impairments in the domains of attention, Executive
functions, and Memory (Chu et al., 2007; Dikmen et al.,
2009; Haberg et al., 2015; Rabinowitz et al., 2018; Ruttan
et al., 2008; Vasquez, Tomaszczyk, Sharma, Colella, &
Green, 2018). Various publications have demonstrated that
moderate–severe TBI can lead to progressive degenerative
processes affecting neurocognitive functioning (Corrigan &
Hammond, 2013) as well as the development of late medical
effects such as posttraumatic epilepsy (Lowenstein, 2009;
Masel & DeWitt, 2010); thus, some individuals do not achieve
stability in the chronic stages of injury. Unfortunately, individ-
uals with moderate–severe TBI are more at risk for developing
neurological disorders later in life, such as Alzheimer’s dis-
ease, particularly for those with the APOE ε4 genotype
(Edlow et al., 2018; Isoniemi, Tenovuo, Portin, Himanen,
& Kairisto, 2006). However, the effect of APOE ε4 on cog-
nitive functioning was not observed during the early period
of recovery (Padgett, Summers, Vickers, McCormack, &
Skilbeck, 2016).
Studies have reported that individuals with moderate–
severe TBI can decline in cognitive functioning between
the first months and 5 years after injury (Green et al., 2014;
Millis et al., 2001; Till, Colella, Verwegen, & Green, 2008),
at least in some areas of cognitive functioning such as
Memory functions (Till et al., 2008) and Executive function
(Vasquez et al., 2018). Indeed, the degree of variability in cog-
nitive recovery following moderate–severe TBI is exemplified
by Millis et al. (2001), where 22.2% of patients improved,
15.2% declined, and 62.6% were unchanged in neuropsycho-
logical measures 1–5 years after injury. However, long-term
changes or declines were not observed in intellectual function-
ing from 1 year up to 16 years after injury (Wood &
Rutterford, 2006).
Identifying factors associated with neurocognitive out-
comes in chronic TBI when viewed over longer periods is
of importance in order to understand its progression.
Differences in injury severity (Dikmen, Machamer, Powell,
& Temkin, 2003; Draper & Ponsford, 2008) including dura-
tion of posttraumatic amnesia (PTA) (Konigs, de Kieviet, &
Oosterlaan, 2012; Sigurdardottir et al., 2015) have been
shown to influence the recovery of cognitive deficits.
Patient characteristics such as cognitive reserve or premorbid
IQ (Christensen et al., 2008; Leary et al., 2018), education
(Sumowski, Chiaravalloti, Krch, Paxton, & Deluca, 2013),
and age (Kaup et al., 2017; Marquez de la Plata et al., 2008;
Senathi-Raja, Ponsford, & Schonberger, 2010; Wood, 2017)
have been recognized as predictors that were significantly
associated with the cognitive outcomes after TBI. For example,
a high age at injury and male gender were significant risk
factors of cognitive deficits and decline decades after TBI
(Himanen et al., 2006; Senathi-Raja et al., 2010).
Depression and anxiety are the most common psychiatric
problems experienced by patients following TBI (Bombardier,
Hoekstra, Dikmen, & Fann, 2016; Gould, Ponsford, Johnston,
& Schonberger, 2011). Correspondingly, there have been
several longitudinal studies of neuropsychiatric issues
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(anxious/depressed mood) and cognitive outcomes over
10 years after moderate–severe TBI (Dahm & Ponsford,
2015; Grauwmeijer et al., 2018). Grauwmeijer et al.
(2018) showed no strong evidence for associations between
depression and neurocognitive functioning spanning 10 years
post-TBI. Other studies reported that elevated scores on
emotional symptom rating scales (Symptom Checklist-90-R,
Hospital Anxiety and Depression Scale) were related to worse
neurocognitive outcomes up to 10 years after TBI (Dahm &
Ponsford, 2015; Ponsford et al., 2008).
There is still limited research on the long-term cognitive
trajectories following TBI. Inconsistent findings, partly due
to the heterogeneity of TBI and different assessment methods
used in the studies, challenge our understanding of the
chronicity of cognitive difficulties after moderate–severe
TBI. Thus, well-designed, longitudinal studies with large
samples are still needed. The current study contributes to
the literature by expanding our previous research of the
1 year follow-up after TBI (Sigurdardottir, Andelic, Roe, &
Schanke, 2009) and exploring the changes in scores in neu-
rocognitive domains (Memory, Executive functions, and
Reasoning) across 10 years postinjury in individuals with
moderate–severe TBI. A central aim is to investigate
whether these changes are related to injury severity, dem-
ographics, functional outcome at 3 months postinjury, and
emotional distress at 1 year postinjury. Memory and
Executive function were included because these domains
are most likely to be affected following TBI (Kersel,
Marsh, Havill, & Sleigh, 2001). Other TBI studies using
IQ assessments have found that general intelligence was
significantly lower in individuals with TBI compared to
healthy controls (Donders, Tulsky, & Zhu, 2001; Konigs
et al., 2012; Rassovsky et al., 2015). In order to investigate
the influence of injury severity characteristics on trajectory
of intellectual abilities, the Reasoning domain was
included in this longitudinal study. In addition, this study
aims to investigate whether neuropsychological performance
remained stable or changed in the chronic phase from 1 year
to later follow-ups (5 or 10 years). Based on the current liter-
ature, it was hypothesized that neurocognitive functioning
would be significantly improved over time. It was expected
that education and injury severity would significantly predict
long-term neurocognitive functioning. In order to identify
individuals manifesting cognitive decline by using a Reliable
Change Index (RCI), it was hypothesized that decline might
appear within Memory and Executive function but not in
Reasoning in the long-term perspective.
METHODS
Design
This study was a longitudinal prospective study of individ-
uals with acute TBI admitted from 2005 to 2007 to the
Trauma Referral Centre at Oslo University Hospital, Oslo,
Norway. Participants had four follow-ups over 10 years
 Trajectory of 10-Year Neurocognitive Functioning 3

Eligibility: Persons with moderate-to-severe TBI admied to

the Oslo University Hospital May 2005–May 2007
N = 147

Deceased in the acute

phase (n = 24)

Confirmed eligible: Persons who received

informaon about the study 4–6 weeks post-injury
N = 123

Refusal, non-responders Ongoing PTA > 6 months

(n = 29) (n = 11)

Deceased btwn 1-10 year

follow-up (n = 4)

Completed baseline assessment

N = 79

Withdrew from study (n = 1) Missing 1-year data (n = 4)

1-year follow-up
N = 74

Withdrew from study (n = 5)

5-year follow-up
N = 69
Withdrew, did not show up Living abroad, sickness,
(n = 10) unable to contact (n = 6)
10-year follow-up
N = 53

Fig. 1. Patient eligibility flowchart and follow-ups.

with neuropsychological assessments at 3 months, 1, 5, and
10 years postinjury.
Study population
The criteria for inclusion were (a) persons 16–55 years of age;
(b) residing in East region of Norway; (c) admitted with the
following ICD-10 diagnoses within 24 h of injury: contu-
sions/diffuse brain lesions (S06.1–S06.3, S06.7–S06.9,
S07.0, S07.1, S09.7, T04.0, and T06.0), traumatic intracra-
nial hemorrhages (S06.4–S06.6), cranial fractures (S02.0,
S02.1, and S02.7–S02.9), and concussions (S06.0) (see
Andelic, Sigurdardottir, Brunborg, & Roe, 2008); and (d)
computed tomography (CT) brain scan performed within
24 h postinjury. Patients with a diagnosis expected to inter-
fere with TBI-related outcome were excluded: (a) previous
neurological disorders; (b) associated spinal cord injuries;
and (c) severe psychiatric or substance use disorders. The ini-
tial severity of TBI was measured by the Glasgow Coma
Scale (GCS) (Teasdale & Jennett, 1974), with scores of
3–8 (severe TBI) and 9–12 (moderate TBI) given on admis-
sion to the emergency department at the hospital or preintu-
bation values assigned at the accident site. Eligibility criteria
for the neuropsychological study included patients who had a
Galveston Orientation and Amnesia Test (GOAT) (Levin,
O’Donnell, & Grossman, 1979) score of more than 75 and
speaking the Norwegian language.
Eligible participants between 16 and 55 years old received
a letter containing information about the study 4–6 weeks
after injury. A total of 147 persons with moderate–severe
TBI were eligible during the inclusion period of 2005–2007.
Twenty-four persons died in acute and postacute care and
four died between 1 and 10 year follow-ups. Eleven persons
who had ongoing PTA or were in a vegetative state during
the first year were excluded. Twenty-nine persons declined
to participate. The final sample included 79 patients
(61 males and 18 females) for a 10 year analysis in this study
(see Figure 1).
Evaluations were conducted at the outpatient TBI depart-
ment of the Oslo University Hospital, Oslo, Norway, or dur-
ing the rehabilitation stay at the Sunnaas Rehabilitation
Hospital, Nesodden, Norway, between August 2005 and
February 2017. Participants completed a neuropsychological
examination before they completed a set of questionnaires.
The examination duration was approximately 3 hr. Written
consent was obtained from all participants. No control group
was used in this study. The Regional Committee for Medical
Research Ethics, East-Norway, and the Norwegian Data
Inspectorate approved the study according to the Helsinki
Declaration.

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 4 S. Sigurdardottir et al.
Measures
Assessment of clinical and trauma status
Demographic variables (age, gender, education, employ-
ment, and marital status) were collected at 3-month follow-
up. Employment preinjury was dichotomized into employed
and unemployed, where individuals in the employed group
consisted of individuals working full/part time or studying
(high school, college, or university), while those in the unem-
ployed group were jobseekers, on sick leave, or receiving dis-
ability pension. Marital status was dichotomized into married/
partnered and single.
Trauma scores of the Abbreviated Injury Scale (AIS)
(Association for the Advancement of Automotive Medicine,
1990) and Injury Severity Score (ISS) (Baker, O’Neill,
Haddon, & Long, 1974) were extracted from the Trauma
Registry at the Oslo University Hospital, Ulleval. AIShead
scores ranged from one (minor) to six (fatal). An ISS score
greater than 15 (ranging from 1 to 75) was accepted as the
definition of a major trauma patient.
Duration of PTA was chosen as a measure of injury
severity because it is most often used by rehabilitation physi-
cians when making prognostic evaluations (Ponsford, Spitz, &
McKenzie, 2016). A GOAT score above 75 indicated emer-
gence from PTA. PTA was evaluated on a daily basis during
rehabilitation in 89% of cases with severe TBI and 45% of
those with moderate TBI. Four patients with severe TBI had
PTA lasting longer than 3 months and were therefore assessed
with neuropsychological measures at 5 months postinjury. For
20 patients (25%), duration of PTA was obtained from medical
records.
Assessment of emotional distress
The Symptom Checklist 90-Revised (SCL-90-R) (Derogatis,
1983) measured 90 symptoms during the previous 7 days on a
5-point scale from 0 (not at all) to 4 (extremely). The 90 scores
were transferred to a profile sheet of nine symptom dimen-
sions (Somatization, Obsessive-Compulsive, Interpersonal
Sensitivity, Depression, Anxiety, Hostility, Phobic Anxiety,
Paranoid Ideation, and Psychoticism) and provided a Global
Severity Index (GSI) that represents overall psychological
distress. The SCL-90-R was collected at 3-month and 1-year
follow-ups. Because of the lack of awareness in the early
stage after brain injury (Geytenbeek, Fleming, Doig, &
Ownsworth, 2017) we chose to include the GSI score at
1 year to predict trajectories of long-term cognitive outcomes.
The demographically corrected T-score was used (Derogatis,
1983), and a higher score was indicative of greater emotional
distress. The effects of depression, comorbid psychiatric
disorders, medication, and substance abuse on neurocogni-
tive outcomes were not examined in the current study
because of insufficient statistical power for multiple predic-
tor analysis. Further details about psychiatric disorders,
including depression, anxiety, and substance abuse, have
been published elsewhere (Sigurdardottir, Andelic, Roe, &
Schanke, 2013).
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Assessment of functional status
The Glasgow Outcome Scale-Extended (GOSE) is a struc-
tured interview for assessing areas of independence, work,
leisure activities, and participation in social life (Wilson,
Pettigrew, & Teasdale, 1998). The GOSE scores represent
the following: 1 = dead, 2 = vegetative state, 3 and 4 =
lower/upper severe disability, 5 and 6 = lower/upper moder-
ate disability, 7 and 8 = lower/upper good recovery. A GOSE
score ≥ 6 indicates that people are able to participate in a
working environment or studying (Wilson et al., 1998).
GOSE measured at 3 months was chosen because this time
point has been shown to predict long-term neuropsychologi-
cal deficits better than GOSE measured at early hospital dis-
charge (Gautschi et al., 2013).
Assessment of neurocognitive domains
Neuropsychological evaluations were performed at 3-month,
and at 1-, 5-, and 10-year follow-ups. Neuropsychological
raw scores were transformed to standardized scores accord-
ing to age- and gender-corrected normative data. Normative
data were not stratified by education. The tests included in
each domain were based on data in the literature and were
among the tests most commonly used by clinical neuropsy-
chologists regarding TBI (Rabin, Barr, & Burton, 2005).
Memory domain. The California Verbal Learning Test-II
(CVLT-II; List A trials 1–5) (Delis, Kaplan, Kramer, &
Ober, 2000) was administered to assess learning and memory
using the sum of correctly recalled words (List A trials 1–5).
The Rey–Osterrieth Complex Figure Test (ROCF) (Meyers
& Meyers, 1995) measured visual–spatial constructional abil-
ity and visual memory, wherein the participant copies a com-
plex figure and draws the same figure from memory. Only the
short delay task (ca. 3 min) was used in this study. Results
from both the CVLT-II (List A) (Delis et al., 2000) and
ROCF (Meyers & Meyers, 1995) were given by a T-score
(M = 50, SD = 10).
Executive function domain. The subtests of the Letter
Fluency Task and Color-Word Interference Test (CWIT,
condition 3) from the Delis–Kaplan Executive Function
System (D-KEFS; Delis, Kaplan, & Kramer, 2001) were
administered to assess phonemic word fluency, inhibition,
and mental flexibility. The Letter-Number Sequencing from
the Wechsler Adult Intelligence Scale Third Edition (WAIS-
III; Wechsler, 1997) was included to assess verbal working
memory and divided attention. The Trail Making Test, Part
B (Reitan & Wolfson, 1985) was administered as a measure
of mental flexibility.
Reasoning (intellectual) domain. The intelligence/reasoning
level was assessed by administering the subtests Similarities
and Matrices of the WAIS-III (Wechsler, 1997).
 Trajectory of 10-Year Neurocognitive Functioning 5

Statistical analysis Table 1. Demographics, patient characteristics, and symptom scores

of the follow-up sample (N = 79)
Statistical analyses were performed using IBM SPSS, version
23 (SPSS Inc., Chicago, IL, USA). Descriptive analyses of Follow-ups (baseline at 3 months) N = 79
demographic, clinical, and neuropsychological tests were per- 1 year 74 (94%)
formed. The subtask scores of the D-KEFS and WAIS-III were 5 year 69 (87%)
scaled scores (M = 10, SD = 3), which were converted into 10 year 53 (67%)
T-scores before a composite score was calculated within each Demographics
domain (Memory, Executive function, and Reasoning). The Age at injury (range 16–52) 30.2 (10.5)
Shapiro–Wilk test showed that the neuropsychological Education years (range 8–18) 12.6 (2.3)
T-scores accorded with normal distribution (all p > .05). Gender (male) 61 (77%)
Sample size and statistical power were calculated by the pro- Marital status (single at baseline) 59 (75%)
gram G*power (Faul, Erdfelder, Lang, & Buchner 2007). The Employed/studying preinjury 67 (85%)
Severity characteristics
sample size of 77 would give a statistical power of 0.8 at α
Severe TBI (GCS 3–8) 46 (58%)
level of .05, with large effect size (F2 = 0.26) and six predic- GCS (range 3–12) 7.8 (3.1)
tors. The RCI values were calculated for neurocognitive PTA days (range 0–128) 24.2 (29.6)
composite scores based on the RCI described by Jacobson Abbreviated Injury Scalehead (range 2–5) 4.3 (1.0)
and Truax (Jacobson & Truax, 1991). Change was defined Injury Severity Score (range 5–59) 29.4 (13.5)
by RCI values ±1.645 (a 2-tailed α of 0.10, with a 90% con- External cause of injury (traffic accidents) 45 (57%)
fidence interval) as recommended by Duff (2012). For each Clinical variables
neurocognitive domain, the number of participants with GOSE at 3 months (range 3–7) 5.4 (0.8)
improved (positive values) or declined (negative values) per- GOSE at 10 years (range 4–8) 6.2 (1.2)
formance over the years was counted, that is, between 1 and SCL-90-R GSI at 3 months (range 39–131) 55.8 (17.1)
5 years and between 1 and 10 years. SCL-90-R GSI at 1 year (range 40–113) 55.3 (14.2)
A hierarchical linear modeling (HLM) analysis was used GCS = Glasgow Coma Scale; PTA = posttraumatic amnesia; GOSE = Glasgow
to examine predictors for the three separate models of Outcome Scale-Extended; SCL-90-R: Symptom Checklist 90-Revised.
Memory, Executive function, and Reasoning. Neurocognitive Note: Values are mean (SD) or n (%).
composite scores were used as dependent variables with four
time points coded as 0.25 (3 months), 1 (1 year), 5 (5 years),
and 10 (10 years). First, models were run without covariates
RESULTS
to establish the best-fitting model. When the most accurate
curvature model was determined, the covariates were then Patients’ characteristics
included in the models: age, education, duration of PTA,
AIShead, general functioning (GOSE) at 3 months, and self- Table 1 presents the general characteristics and injury-related
reports of emotional distress (SCL-90-R: GSI) at 1 year. data of the 79 participants. The majority of participants were
Since the correlation between ISS and AIShead was high male (77%) and single (75%) and were working or studying
(r = .71), the AIShead was preferred as a measure of brain at the time of injury (85%). The mean age was 30.2 years
injury severity. The Pearson correlation coefficient between (range 16–52), and the mean years of education was
PTA and AIShead was r = .36. Covariate data were entered 12.6 years (range 8–18). Education is presented as a continu-
simultaneously as fixed effects. A random intercept was ous variable in Table 1 but was categorized as 9–12 years or
included for the patient neuropsychological performance, ≥13 years of education, based on the mean values before
and the interactions between follow-up time and significant being entered into the HLM analyses.
predictors in each model were then modeled. Continuous pre- According to the GCS, 46 participants sustained a severe
dictor variables were centralized with the total sample mean TBI (GCS 3–8). For the total sample, PTA ranged from 0 to
values before being entered into the HLM. The model handled 128 days. The AIS scores ranged from 2 to 5 and the ISS
missing data at the follow-ups through maximum likelihood scores ranged from 5 to 59. A traffic accident was the cause
estimation, thus retaining all 79 patients. Statistically sig- of injury in more than half of the injuries. As reflected by the
nificant fixed effects on the Memory, Executive function, GOSE mean scores at both the 3-month (range 3–7) and
and Reasoning composite scores were then graphed across 10-year follow-ups (range 5–8), the functional levels were
each of the time points. The main effects would indicate consistent with lower and upper moderate disability, respec-
that the composite scores over time vary as a function of tively. Participants did not report severe symptoms according
the predictor variable. Cohen’s d effect sizes were calculated to the mean scores of the SCL-90-R at the 3-month (range
for the neuropsychological tests between the first and last assess- 39–131) and 1-year (range 40–113) follow-ups.
ment follow-ups, interpreted as small = 0.10, medium = 0.30, Results of sensitivity analyses comparing the participants
and large = 0.50 (Cohen, 1992). The statistical significance followed up at 10 years (n = 53) and those who dropped out
was set at p < .05. in the study (n = 26) did not show significant differences with

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 6 S. Sigurdardottir et al.
respect to age t = −0.492, p = .624, education t = 0.869,
p = .387, PTA t = 0.709, p = .481, AIShead t = 1.492,
p = .140, or GOSE at 3 months t = −0.937, p = .352. These
characteristics were similar for the participants and dropouts.
Of note, the SCL-90-R GSI at 3 months was statistically sig-
nificant between the groups t = −2.029, p = .046, and the
SCL-90-R GSI at 1 year approached marginal significance
t = −1.714, p = .091. Those in the dropout group were more
likely to report emotional distress than the participants.
Neurocognitive performance over time
Descriptive statistics for neuropsychological scores at each
follow-up (i.e., 3 months, 1, 5, and 10 years) are presented
in Table 2. At 3 months, the TBI sample showed 1 SD below
average in composite scores of Memory and Executive func-
tion and 0.5 SD below average in the composite score of
Reasoning. As seen in Table 2, the mean Memory composite
scores increased from 38.2 (SD 11.6) at 3 months to 45.4
(SD 13.2) at 10 years; the mean Executive function composite
scores increased from 38.7 (SD 7.9) to 43.7 (SD 7.3) between
the same follow-ups; and the mean Reasoning composite
scores increased from 44.6 (SD 8.4) to 47.3 (SD 8.1). The
effect sizes between the first (3 months) and last (10-year)
follow-up assessments were large for the Memory domain
(Cohen’s d range: 0.44–0.57), followed by small to large
effect sizes for the Executive domain (Cohen’s d range:
0.17–0.70), and small to moderate effect sizes for the
Reasoning domain (Cohen’s d range: 0.15–0.44), across
age and gender groups.
Pearson correlation coefficients between three neurocog-
nitive trajectories were as follows: Memory and Executive
function r = .66; Memory and Reasoning r = .51; and
Executive function and Reasoning r = .57.
Between the 1 and 10 year follow-ups, the neuropsycho-
logical composite scores were fairly stable at the mean group
level. Using the RCI, as in other TBI studies (Bercaw, Hanks,
Millis, & Gola, 2011; Till et al., 2008), approximately
83–96% of individuals remained cognitively stable between
1 and 10 years (see Table 2). The RCI was calculated between
the 1 year and later follow-ups, that is, participants who
attended either the 5 year (n = 62) or 10 year follow-ups
(n = 47). A significant increase was observed in 2–6% of
participants (n = 47) from 1 to 10 year follow-ups across
the three neurocognitive domains, and a significant decrease
was observed in 2–11%. Decreased performance was most
frequently observed (11%) within the Memory domain.
Predictors of neurocognitive trajectories
Unconditional Models (i.e., no covariates)
The first analyses examined if there was a large enough score
variance within subjects to proceed with the HLM. The
Memory model showed a significant estimated subject vari-
ance of 109.00 (Wald Z = 3.98, p < .001) and a significant
estimated residual variance of 41.13 (Wald Z = 9.72,
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p < .001); the Executive function model showed a significant
estimated subject variance of 47.31 (Wald Z = 5.70, p < .001)
and a significant estimated residual variance of 15.10 (Wald
Z = 9.70, p < .001); and the Reasoning model showed a sig-
nificant estimated subject variance of 48.26 (Wald Z = 5.66,
p < .001) and a significant estimated residual variance of
16.71 (Wald Z = 9.68, p < .001). The results indicate a wide
change in neurocognitive scores over time. A spaghetti plot of
79 participants demonstrated an inter-individual variability in
Memory scores (see Supplementary Figure).
Model fit
Unconditional linear, quadratic, and cubic models were then
analyzed without the covariates for each neurocognitive
domain scores over time, but including the quadratic and
cubic effects did not improve model-fit based on -2 log like-
lihood (-2LL), Akaike information criterion, and Bayesian
information criterion (see Table 3). A linear shape trajectory
emerged as the best fitting to the data in the neurocognitive
analyses over time.
Full models
Demographic, injury severity, functional outcome, and self-
reported symptom covariates in the models of domain-
specific neurocognitive trajectories (Memory, Executive
function, and Reasoning) are presented in Table 4, which
shows their standardized coefficients (β) and statistically
significant and nonsignificant fixed effects from the HLM,
as well as 95% confidence intervals. Details of the distribu-
tion of changes in the neurocognitive T-scores by predictors
are presented in the Supplementary Table.
As seen in Table 4, a significant improvement in perfor-
mance over time was found between 3 months and 1 year
(all three neurocognitive trajectories p < .01). A higher level
of education was significantly associated with a better perfor-
mance on the neurocognitive trajectories, with the strongest
association with Reasoning (p < .001). Those with fewer
symptoms of emotional distress (SCL-90-R) also performed
better on the neurocognitive trajectories (ps < .05). Participants
with a shorter duration of PTA (p = .009) showed a better
performance on Memory. Individuals with better functional
outcome (p = .040) showed better performances on Memory
and Executive function. To illustrate the effects of the
demographics and clinical predictors, Figure 2 displays the
neurocognitive trajectories that were estimated based on a
mean-split procedure (above and below the mean) for the
PTA, GOSE, SCL-90-R, and education. For example, the
GOSE mean score was 5.4 at 3 months and was dichotomized
into GOSE scores ≤ 5 and scores ≥ 6 to be plotted across the
four time points. There were no statistically significant inter-
actions of any predictors with the neurocognitive trajectories
over time (see Table 4). This suggests that the slopes of the
subjects’ neurocognitive trajectories did not differ over time
as a function of education, injury severity, emotional distress,
and functional outcome.
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Trajectory of 10-Year Neurocognitive Functioning

Table 2. The three neurocognitive composite scores and neuropsychological tests from 3 months to 10-year follow-up (N = 79)

Follow-ups postinjury Individual change in performancea

Stable Improved Declined Stable Improved Declined
3 months 1 year 5 year 10 year (1–5 years) (1–5 years) (1–5 years) (1–10 years) (1–10 years) (1–10 years)
Neuropsychological variable (n = 79) (n = 74) (n = 69) (n = 53) (n = 62) (n = 62) (n = 62) (n = 47) (n = 47) (n = 47)
Memory composite, mean (±SD) 38.2 (11.6) 45.7 (12.4) 44.1 (11.6) 45.4 (13.2) 90% 0% 10% 83% 6% 11%
Memory composite, median (range) 38 (14–65) 47 (16–68) 46 (17–65) 46 (20–69)
CVLT-II Total trials 1–5, mean (±SD) 39.4 (13.2) 45.6 (12.9) 42.0 (11.5) 44.8 (12.8)
ROCF short-term, mean (±SD) 37.0 (14.8) 45.8 (15.4) 46.2 (15.6) 46.0 (17.0)
Executive Function composite, mean (±SD) 38.7 (7.9) 41.9 (7.6) 42.4 (8.2) 43.7 (7.3) 98% 0% 2% 96% 2% 2%
Executive Function composite, median (range) 39 (22–52) 42 (22–59) 44 (23–58) 45 (27–61)
D-KEFS Verbal Fluency Test, mean (±SD) 40.1 (10.7) 44.9 (11.8) 45.3 (12.1) 48.0 (11.9)
D-KEFS CWIT Condition 3, mean (±SD) 39.7 (12.8) 43.1 (12.3) 43.9 (11.8) 45.3 (10.6)
WAIS-III Letter-Number Seq., mean (±SD) 38.1 (8.9) 39.5 (8.3) 39.4 (8.8) 39.5 (7.4)
Trail Making Test B, mean (±SD) 34.7 (11.8) 37.4 (12.5) 41.1 (10.8) 41.8 (10.3)
Reasoning composite, mean (±SD) 44.6 (8.4) 47.4 (8.5) 47.9 (7.1) 47.3 (8.1) 95% 0% 5% 94% 2% 4%
Reasoning composite, median (range) 44 (29–65) 47 (30–67) 49 (30–63) 48 (29–67)
WAIS-III Matrix Reasoning, mean (±SD) 47.3 (11.1) 50.6 (11.4) 51.6 (10.0) 52.2 (11.2)
WAIS-III Similarities, mean (±SD) 41.3 (8.2) 43.2 (8.6) 43.9 (8.0) 42.5 (7.8)

CVLT-II = California Verbal Learning Test-II; ROCF = Rey–Osterrieth Complex Figure Test; D-KEFS = Delis–Kaplan Executive Function System; CWIT = Color-Word Interference Test; WAIS-III = Wechsler Adult
Intelligence Scale-Third Edition.
Note: Values are T-scores.
a
Based on the Reliable Change Index for neurocognitive composite T-scores between 1 year and later follow-ups (i.e., participants who attended either the 5-year or 10-year follow-ups).

7
 8 S. Sigurdardottir et al.
Table 3. Model fit for neurocognitive trajectories over
time
Model memory −2 Log likelihood
Linear 1895.42
Quadratic 1906.15
Cubic 1913.61
Model Executive
Linear 1622.46
Quadratic 1631.00
Cubic 1639.20
Model Reasoning
Linear 1676.90
Quadratic 1681.21
Cubic 1684.17
Note: The Chi-square value for significant difference (p = .05)
is ≥ 3.84 drop from the previous model. Lower −2 log like-
lihood is better.
DISCUSSION
This study examined the trajectory of neurocognitive perfor-
mance over the course of 10 years in patients with moderate–
severe TBI. Follow-up assessments were conducted at
3 months, 1, 5, and 10 years postinjury. The findings demon-
strate that significant changes were observed in all neurocog-
nitive domains (Memory, Executive function, and Reasoning),
with the greatest improvement occurring during the first year
postinjury, in line with previous TBI studies (Christensen
et al., 2008; Rabinowitz et al., 2018; Sigurdardottir et al.,
2009; Spitz, Ponsford, Rudzki, & Maller, 2012). After the
first year, cognitive stability up to 10 years after injury was
observed among the majority of patients who retained in this
study. However, one-third of the participants dropped out and
this may limit the study generalizability. Other longitudinal
studies (Millis et al., 2001; Ruttan et al., 2008; Till et al.,
2008) and a recent review (Mollayeva, Mollayeva, Pacheco,
D’Souza, & Colantonio, 2019) examining neurocognitive func-
tioning in mixed TBI populations indicated trends in functioning
stability after the first year after trauma, which may give reason
for optimism. However, a small subset of patients (11%) in this
study showed a significant decline, especially in memory perfor-
mance. Perhaps this decline was not apparent until sufficient
time had passed, that is, up to 5–10 years after trauma.
Previous findings by Ruff et al. (1991) reported that 33%
of those with severe TBI declined in verbal memory from
6 to 12 months postinjury (Ruff et al., 1991). A systematic
review on moderate–severe TBI recommended that regular
assessments should be made every 3–5 years to detect
long-term cognitive changes (Schultz & Tate, 2013). Such
follow-ups may also assist in the aid of differential diagnoses
for the TBI population. Other longitudinal studies following
moderate–severe TBI have reported neurocognitive decline
at various time points after injury from 2 years up to 5 years
(Hammond, Hart, Bushnik, Corrigan, & Sasser, 2004; Till
et al., 2008) and as long as 30 years (Himanen et al., 2006).
A prior study found that 14%, 26%, and 61% of 292 patients
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with TBI demonstrated declines, improvements, or no
change, respectively, between 1 and 5 years after injury
(Hammond et al., 2004). Importantly, hours of rehabilita-
tion in early phases were shown to have the greatest effect
on later cognitive decline (Till et al., 2008). These findings
may have clinical value for a specific subgroup of patients,
indicating the need for continual neurocognitive assessments
and for seeking age-related changes including psychological
(e.g., depression and anxiety) and medical (e.g., seizures,
biomarkers, and neurodegenerative) mechanisms that may
contribute to cognitive decline in chronic TBI. However,
as the time since TBI progresses, the environmental, behav-
ioral, structural, morphological, and physiological influences
may become a scientific challenge in understanding the
prognostic factors of cognitive outcomes (for review, see
Mollayeva et al., 2019). The current findings suggest that
premorbid relationship of education was a consistently sig-
nificant predictor of the three neurocognitive trajectories,
where individuals with a lower education (12 years or less)
showed a trend in Reasoning decline after 5 years of brain
trauma (e.g., see Figure 2). However, the interaction effects
between time and education in predicting neurocognitive
trajectories were nonsignificant. Sumowski et al. (2013) pre-
sented that a higher education level may have neuroprotective
effects when facing TBI, while Miller, Colella, Mikulis,
Maller and Green (2013) found that preinjury education
was not associated with hippocampal neurodegeneration in
the chronic stages of moderate–severe TBI.
Another study offered support for the cognitive reserve
(i.e., preinjury intellectual functioning) in predicting cognitive,
occupational, emotional, and social outcomes (Rassovsky et al.,
2015). Furthermore, one study found that persons with a college
education (i.e., a better cognitive reserve) were seven times more
likely than those who did not finish high school to be disability-
free 1 year after a TBI (Schneider et al., 2014). In the present
study, significant improvement was evident in the Reasoning
trajectory (WAIS-III: Similarities, Matrices) occurring between
3 months and 1 year, with scores returning to the average range
at 1 year, suggesting that Reasoning abilities are relatively robust
after moderate–severe TBI.
This study is one of few TBI studies that investigated
neurocognitive trajectories across 10 years in adults. We identi-
fied differential contributions of injury severity and clinical
variables in the association of neurocognitive domains. Of
all included predictors, the most notable association with
the Memory trajectory was the duration of PTA, that is, a dura-
tion longer than 3 weeks was negatively associated with a worse
memory performance. A recent study of patients with moderate–
severe TBI did not find age, education, or injury severity (GCS
score) as predictors of visual memory change from 3 to
12 months follow-up (Zaninotto et al., 2017). The length of
PTA as a measure of injury severity is known to affect cognitive
and intellectual functioning both in the acute and postacute
phases of TBI (Konigs et al., 2012; Ponsford et al., 2016;
Rassovsky et al., 2015). Studies of severe TBI have suggested
a PTA duration of 4 weeks as a threshold for predicting cogni-
tive outcomes (Brown et al., 2010; Sigurdardottir et al., 2015).
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Trajectory of 10-Year Neurocognitive Functioning

Table 4. Predictors of each neurocognitive trajectory across 3 months, 1-, 5-, and 10-year follow-ups

Memory Executive function Reasoning

Lower bound Upper bound Lower bound Upper bound Lower bound Upper bound
Predictor variable β SE p (95%CI) (95%CI) β SE p (95%CI) (95%CI) β SE p (95%CI) (95%CI)
Intercept 44.94 1.43 .001* 42.07 47.80 43.12 0.77 .001* 41.63 44.70 47.18 0.89 .001* 45.40 48.96
Time of assessment
3 months −5.94 1.33 .001* −8.59 −3.28 −4.02 0.75 .001* −5.53 −2.51 −2.46 0.76 .002* −3.98 −0.94
1 year 0.72 1.09 .512 −1.47 2.90 −1.10 0.67 .110 −2.43 0.26 0.16 0.72 .874 −1.34 1.57
5 year −1.19 0.97 .226 −3.14 0.76 −0.55 0.64 .399 −1.83 0.74 0.06 0.67 .928 −1.29 1.41
10 year 0a 0 – – – 0a 0 – – – 0a 0 – – –
Age 0.16 0.09 .091 −0.03 0.34 0.14 0.07 .048 −0.00 0.28 0.07 0.07 .350 −0.08 0.22
Education 0.94 0.43 .031* 0.09 1.80 1.15 0.31 .001* 0.52 1.78 1.43 0.34 .001* 0.75 2.11
PTA −0.12 0.04 .009* −0.21 −0.03 0.02 0.03 .628 −0.05 0.08 −0.01 0.03 .876 −0.08 0.06
AIShead −0.77 1.19 .519 −3.15 1.61 −1.79 0.88 .046* −3.55 −0.04 0.35 0.94 .707 −1.53 2.24
GOSE 3 months postinjury 3.39 1.43 .021* 0.53 6.26 2.21 1.06 .040* 0.10 4.32 1.35 1.13 .237 −0.90 3.61
SCL-90-R 1 year postinjury −0.21 0.07 .006* −0.36 −0.06 −0.19 0.06 .001* −0.23 −0.08 −0.13 0.06 .030* −0.25 −0.01
-2LL without interaction 1578.0 1371.1 1422.0
Time × Significant predictors
Time × Education 0.12 0.08 .111 −0.03 0.27 0.07 0.05 .199 −0.04 0.17 −0.00 0.05 .967 −0.11 0.10
Time × PTA 0.00 0.01 .618 −0.01 0.02 – – – – – – – – – –
Time × AIShead – – – – – 0.00 0.17 .966 −0.32 0.33 – – – – –
Time × GOSE −0.08 0.28 .781 −0.62 0.47 −0.06 0.17 .734 -0.40 0.28 – – – – –
Time × SCL-90-R −0.00 0.01 .820 −0.03 0.03 0.00 0.01 .934 −0.02 0.02 −0.00 0.01 .977 −0.02 0.02
−2LL with interaction 1733.5 1573.6 1675.7

PTA = posttraumatic amnesia; AIShead = Abbreviated Injury Scalehead GOSE = Glasgow Outcome Scale-Extended; SCL-90-R = Symptom Checklist 90-Revised.
Note: Predictor variables are centered at mean. Lower scores on the Abbreviated Injury Scale indicate less severity. Lower scores on the SCL-90-R indicate less distress. Higher scores on the GOSE indicate better functional
outcome.
*p < .05.
a
Set to zero because of redundant.

9
 10
Fig. 2. Neuropsychological trajectories by significant predictors for the three cognitive domains. Cognitive composite score are presented by
T-scores (mean, standard error). PTA = posttraumatic amnesia; GOSE = Glasgow Outcome Scale-Extended; SCL-90-R = Symptom
Checklist 90-Revised.
The current study indicates that greater deficits in Executive
function were related to early emotional distress and functional
impairment; however, the nature of these relationships is
unclear. Executive function difficulties may have led to
emotional or behavioral problems, further affecting school
or work outcomes (general functioning). In the present study,
emotional distress symptoms measured at 1 year postinjury
predicted all neurocognitive trajectories. Prior research
reported that patients with diagnosed anxiety disorders post
moderate–severe TBI had a significantly slower information
processing speed, a worse working Memory, and worse
Executive functions compared to those without postinjury
anxiety (Gould, Ponsford, & Spitz, 2014). These same
authors gave support to the theory that cognitive difficulties
could give rise to elevated anxiety after TBI (Schonberger,
Ponsford, Gould, & Johnston, 2011). Other publications have
demonstrated that emotional variables may be accurate in
predicting cognitive outcomes (Grauwmeijer et al., 2018;
Shields, Moons, Tewell, & Yonelinas, 2016). Another study
compared cognitive functioning and emotional distress in
patients with mild–severe TBI at 10 years and found that
the group with a worse functional outcome (GOSE) performed
more poorly on cognitive measures (information processing
speed, attention, Memory, and Executive function) and showed
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S. Sigurdardottir et al.
higher levels of anxiety (Ponsford et al., 2008). In our results, the
functional outcome at 3 months (GOSE) was associated with
both the Memory and Executive function trajectories.
Another study on severe TBI showed that a better functional
outcome at rehabilitation discharge (median of 3 months) was
related to better neuropsychological functioning at a
long-term follow-up (median 20.5 months) (Gautschi et al.,
2013). On the other hand, numerous studies have shown that
common measures of Executive functions (Spitz et al., 2012)
and memory (Bercaw et al., 2011) are important predictors of
functional outcome after TBI.
A recent review by Mollayeva et al. (2019) indicated that
age as a determinant of cognitive outcome is inconsistent.
In the current study, age was not found to be a significant
predictor of neurocognitive trajectories. Another study using
samples of younger to older aged adults (16–81 years)
showed that older adults had poorer cognitive outcomes
across all measures of cognitive domains (Senathi-Raja
et al., 2010). Rabinowitz et al. (2018) also found that age
moderated the recovery trajectory of processing speed index
and the Executive function composite score. The present
study included persons aged 16–55 years at the time of injury,
which may underscore the relationship between age and
long-term cognitive outcome in TBI. Future research with
 Trajectory of 10-Year Neurocognitive Functioning
longitudinal follow-up including older adults where memory
decline becomes clinically apparent is also necessary in the
TBI literature.
Multiplicity concerns may arise in this study due to the
multiple composite scores and the number of analyses. The
HLM analyses were not adjusted for multiple comparisons,
which may inflate the Type I error. It may also be difficult
to interpret the clinical relevance of a small but statistically
significant individual decline in the mean values over time,
and whether this negative result induces further cognitive
evaluation and relevant treatment for the individual. A recent
review of cognitive measures in TBI (D’Souza et al., 2019)
revealed that there is insufficient evidence for the test–retest
reliability and responsiveness of instruments for measuring
longitudinal change in cognition in TBI samples. Unfortunately,
this may apply for the majority of neuropsychological tests
used in this study, and we can question if there was a decline
or a period of stability in cognitive functioning. Much future
research is needed in this area.
Our findings may provide information regarding those
who are most likely to require long-term treatments and
follow-ups, including community rehabilitation of cognitive
abilities (e.g., planning, inhibitory control, and memory),
medical treatment, and psychotherapy. It is unclear if risk
factors for cognitive decline may be education-specific or
if those with lower education have greater risks for repeated
brain injuries with the passing of time, and this should be con-
sidered in future studies. It is also possible that those with a
higher education more often returned to work and had more
access to financial and social support than those with a lower
education. Finally, emotional distress symptoms were associ-
ated with a poorer cognitive performance, making the treat-
ment of psychiatric disturbances an area of high importance
to TBI rehabilitation and in the community.
This study has several limitations. The current sample has
limited age groups (age 16–55 years) and represents generally
severe TBI (58%) with an average PTA duration of 24 days.
Furthermore, the current study needed to rely on medical
records of PTA for 25% of patients, instead of objective ratings
assessed by the GOAT. There was variation in the follow-ups
of the sample, and for some patients, cognitive stability was
assessed between the 1 and 5 year follow-ups, while for others
it was assessed between the 1 and 10 year follow-ups. There
are some limitations to creating a composite score from multi-
ple normative data sets because such a score may contain more
heterogeneity (error variance) than if it was based on a single
sample. Some sample size may be small, limited in hetero-
geneity, or outdated. Furthermore, the composition of
normative samples can have a major effect on the clinical
interpretation of test scores, for example, education, intel-
ligence, and ethnicity (Strauss, Sherman, & Spreen, 2006).
By using the composite scores, it is conceivable that there
is some loss of information. For example, for memory
function, if visuospatial memory declines over time and
verbal memory improves, these could cancel each other
out in the mean composite score. The inclusion of a control
group also would have strengthened the study. One limitation
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11
relates to the possibility of selective attrition. Characteristics
of dropouts did not differ from the participants with regard
to demographics and injury severity measures. However,
results have to be interpreted with caution because selected
variables measured at earlier time points do not guarantee
that these groups are comparable at later follow-ups. In
fact, the SCL-90-R GSI’s p-values at 3 months (p < .05)
and 1 year (p = .09) may indicate the potential for bias
and selective attrition. It is possible that participant attri-
tion may be higher in those reporting increased psycho-
logical distress and this may have affected measures of
association with neurocognitive outcomes.
The strengths of this study include the longitudinal design
of the analysis with four cognitive follow-up time points with
275 observations, and the consistency of the neuropsycho-
logical and clinical evaluations. For the longitudinal cohort,
the attrition rate of 67% over the 10 year study duration was
appreciable (Teague et al., 2018).
In conclusion, the current study demonstrated the
following:
(1) Severity of injury, education, functional outcome, and emo-
tional distress predicted neurocognitive trajectories spanning
10 years after moderate–severe TBI;
(2) As the time since injury progresses, cognitive performance
(Memory, Executive function, and Reasoning abilities) tend
to remain stable for the sample of TBI participants who retained
in the study;
(3) Memory decline was observed over time in a subset of individ-
uals (11%).
ACKNOWLEDGEMENTS
This study was funded by the Department of Research,
Sunnaas Rehabilitation Hospital, Nesoddtangen, and the
Department of Physical Medicine and Rehabilitation, Oslo
University Hospital, Norway. The authors are grateful to
all the persons for their participation. Special thanks to
Tone Jerstad (neuroradiologist, Oslo University Hospital,
Ulleval, Oslo) for the CT assessments and Morten Hestnes
(Trauma Register, Oslo University Hospital, Ulleval, Oslo)
for the extraction of trauma scores.
CONFLICT OF INTEREST
None.
SUPPLEMENTARY MATERIAL
To view supplementary material for this article, please visit
https://doi.org/10.1017/S1355617720000193
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