Child Neuropsychology

A Journal on Normal and Abnormal Development in Childhood and

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ISSN: 0929-7049 (Print) 1744-4136 (Online) Journal homepage: https://www.tandfonline.com/loi/ncny20

Sustained attention and vigilance of children

treated for sagittal and metopic craniosynostosis

Marizela Kljajić, Giovanni Maltese, Peter Tarnow, Peter Sand & Lars Kölby

To cite this article: Marizela Kljajić, Giovanni Maltese, Peter Tarnow, Peter Sand & Lars
Kölby (2019): Sustained attention and vigilance of children treated for sagittal and metopic
craniosynostosis, Child Neuropsychology, DOI: 10.1080/09297049.2019.1682130

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CHILD NEUROPSYCHOLOGY
https://doi.org/10.1080/09297049.2019.1682130

Sustained attention and vigilance of children treated for

sagittal and metopic craniosynostosis
Marizela Kljajića, Giovanni Maltesea, Peter Tarnowa, Peter Sandb and Lars Kölbya
a
Department of Plastic Surgery, Institute of Clinical Sciences, Sahlgrenska, Academy, Göteborg University,
Sahlgrenska University Hospital, Göteborg, Sweden; bDepartment of Psychiatry and Neurochemistry,
Institute of Neuroscience and Physiology, Sahlgrenska Academy, Gothenburg University, Sahlgrenska
University Hospital, Göteborg, Sweden

ABSTRACT ARTICLE HISTORY

Attention problems are common in patients with craniosynostosis. Received 15 April 2019
Craniosynostosis is a rare condition, studies face challenges of selec- Accepted 12 October 2019
tion bias, small sample sizes, and wide age ranges. The aim of the study KEYWORDS
was to assess the sustained attention and vigilance of children treated Craniosynostosis; sagittal
for sagittal and metopic craniosynostosis. To reduce selection bias, we synostosis; metopic
included children that had previously undergone surgery for craniosy- synostosis; attention;
nostosis, were between 8 and 16 years, and lived close to the cranio- vigilance
facial centre. The Connors Continuous Performance Test (3rd edition)
was used to measure sustained attention and vigilance (n = 61;
response rate: 76.3%). Attrition analysis revealed no differences
between responding and non-responding groups regarding back-
ground variables. One identified difference between the SS (n = 28)
and MS (n = 23) groups involved significantly better performance by
the SS group in the hit-reaction time (HRT) test relative to the MS
group (p < 0.05). Compared with the norms, the SS group showed
significantly worse response style, detectability, omissions, commis-
sions, perseverations, HRT response speed (HRT-SD), HRT inter-
stimulus interval change (HRT-iC) (p < 0.01 for all), and variability
(p < 0.05). The MS group showed significantly worse detectability, HRT-
SD, variability (p < 0.01 for all), commissions, perseverations and HRT-iC
(p < 0.05 for all) as compared with norms. No differences regarding
attention was detected for the two different surgical techniques used
for correction of sagittal synostosis. There were shortcomings in sus-
tained attention and vigilance as compared with the norms in the SS
and MS groups, although the deviations were small.

Non-syndromic craniosynostosis (CS) appears in ~1 in 2000 to 2500 births and is caused by

premature closing of one or several sutures, resulting in an atypical head shape. The treatment
for this condition is surgery usually preformed within the first year of life (Mathijssen, 2015).
Long-term outcomes of treatment for CS regarding intellectual development and cognitive
function reveal an increased prevalence of cognitive problems (Bellew & Chumas, 2015;
Bellew, Liddington, Chumas, & Russell, 2011; Chieffo et al., 2010; Hashim et al., 2014; Kapp-
Simon, Leroux, Cunningham, & Speltz, 2005; Kapp-Simon, Speltz, Cunningham, Patel, &

CONTACT Marizela Kljajić marizela.kljajic@vgregion.se Department of Plastic Surgery, Institute of Clinical

Sciences, Sahlgrenska, Academy, Göteborg University, Sahlgrenska University Hospital, Göteborg SE-413 45, Sweden
Supplemental data for this article can be accessed https://doi.org/10.1080/09297049.2019.1682130.
© 2019 Informa UK Limited, trading as Taylor & Francis Group
2 M. KLJAJIĆ ET AL.

Tomita, 2007; Kapp-Simon et al., 2016; Magge, Westerveld, Pruzinsky, & Persing, 2002;
Osborn, Roberts, Mathias, Anderson, & Flapper, 2019; Patel et al., 2014; Speltz, Collett,
Wallace, & Kapp-Simon, 2016; Speltz et al., 2015; Speltz, Kapp-Simon, Cunningham,
Marsh, & Dawson, 2004; van der Vlugt et al., 2012).
Attention as a neuropsychological function of CS has gained increased interest in recent
years and includes several processes, including sensory selection (filter, focus, and alterna-
tion), response selection (response intention, initiative and inhibition, active change, and
executive control), and attentional capacity (effort, sustained performance, and alertness)
(Memoria et al., 2018). Children with CS tend to exhibit decreased attention and lower
executive function relative to controls, although these results were not significant (Collett
et al., 2017). Speltz et al. (2016) found higher average scores for attention problems in the
CS group relative to controls, although these were accompanied by small-to-medium
effects. van der Vlugt et al. (2012) examined a group of metopic CS patients, finding
a 70% versus 24% prevalence of psychopathology in metopic CS patients with an intelli-
gence quotient (IQ) <85 and ≥85, respectively.
Cognitive impairments associated with attention function are often described as
inattention, impulsivity, and over-activity. Additionally, attention-related function is
defined as the ability for sustained attention and vigilance. Measuring attention is
challenging due to its sensitivity to numerous background factors. Attention can
display time-dependent variations depending on how an individual has slept or
eaten, their mental state, and the status of their environment in regard to disturbing
stimuli (Perez-Olmos & Ibanez-Pinilla, 2014). Furthermore, there exist attention-
related problems that are more stable and consistent over longer periods of time,
such as attention deficit/hyperactivity disorder (ADHD). Because there is no diag-
nostic test capable of differentiating the type of attention-related problem(s) present,
it is also (or should be) impossible to diagnose ADHD or any other psychiatric issue
in the absence of a solid anamnesis, given that attention-deficit-related problems
recognized in the everyday life of an individual are a prerequisite for diagnosis
(Austerman, 2015; Wolraich et al., 2011). In clinical practice, continuous perfor-
mance tests (CPT) are often used to assess attention problems. Although it should
not be used as a diagnostic tool, it provides an objective assessment of sustained
attention and vigilance (Berger, Slobodin, & Cassuto, 2017; Lundervold et al., 2016).
One recent study showed that children treated for non-syndromic CS displayed
average cognitive function; however, the results also revealed small impairments in
working memory and processing speed in the group of children treated for sagittal
synostosis (SS). Additionally, background factors in that study showed an increased
incidence of ADHD (Kljajić, Maltese, Tarnow, Sand, & Kölby, 2019). Because impaired
working memory and processing speed can be related to neuropsychological function,
particularly in ADHD and learning disabilities, it is necessary to assess this in association
with CS (Berg, 2008; Brydges, Ozolnieks, & Roberts, 2017).
The aims of the present study were to objectively assess sustained attention and
vigilance of children treated for sagittal and metopic synostosis by using a CPT and to
investigate whether any underlying factor such as IQ, surgical method or presence of
ADHD could affect the outcome.
 CHILD NEUROPSYCHOLOGY 3

Materials and methods

Patients
All patients aged 8 to 16 years, previously operated for sagittal and metopic CS at the
Sahlgrenska Craniofacial Centre, and living in the Västra Götaland or Halland region, i.e.
close to the centre, were invited. Secondary CS and language barriers were exclusion criteria.
The participants were informed by letter and then contacted by phone to schedule an
appointment for assessment by a psychologist. Testing of attention was done as part of
a battery of tests.
Data regarding CS type, surgical method, and age at surgery were extracted from The
Gothenburg Craniofacial Registry, and data regarding cognitive profile (IQ measurement
with Wechsler Intelligence Scale for Children – Fourth Edition (WISC-IV)) was
extracted from a previous study using the same patient cohort (Kljajić et al., 2019).

Ethics
The study was conducted according to the principles stated in the Declaration of Helsinki
and approved by the Gothenburg Ethical Committee (no. 856–13).

Instruments used to measure attention

Connors continuous performance test–3rd edition (Conners CPT 3)
The Connors CPT 3 is a computerized test of attention, where the participant is
instructed to press the spacebar on the keyboard when a letter other than the letter “X”
appears on the screen. The test time is 14 min and includes a total of 360 attempts/trials.
The test comprises 10 variables that measure different aspects (inattentiveness, impulsivity,
and sustained attention and vigilance) of attention-related function: response style, detect-
ability, omissions, commissions, perseverations, hit-reaction time (HRT), HRT response
speed (HRT-SD), variability, HRT block change, and HRT inter-stimulus interval change
(HRT-iC). The interpretation is based on the obtained T-points and described in terms of
attention problems. Higher T-points indicate problems with attention, and lower T-points
indicate a good performance.
The psychometric properties of the Connors CPT 3 have shown a high level of internal
consistency (r: 0.92–0.95). Additionally, test–retest reliability was estimated at an r of 0.67
along with small differences (d: 0.15), indicating a strong reliability and stability over repeated
measurements. Test validity has been assessed according to measurements of discriminative
validity, incremental validity, generalizability, and relationships with intelligence and execu-
tive function. Therefore, the Connors CPT 3 is capable of discriminating between relevant
groups, improving the ability of rating scales for attention in order to accurately predict
ADHD versus general-population groups, generalizability across race/ethnic groups and
nationalities, and returning comparable scores across various settings. Although correlation
analysis has not revealed meaningful associations with general intelligence as assessed by the
Wechsler scale, small associations have been identified with executive function (median r:
0.21) using a normative sample from the United States (n = 1400) extracted from a general-
population sample considering demographic distribution regarding age, gender, race/ethni-
city, parental education level, and region (Connors, 2014).
4 M. KLJAJIĆ ET AL.

Statistical analysis
The distributions of background variables were tested with Fisher’s exact test for dichoto-
mous variables. Mantel-Haenszel chi square test was used for ordered categorical variables
and chi-square test for unordered categorical variables. For continuous variables, the Fisher’s
non-parametric permutation test was used. The same tests were used for attrition analysis.
Comparison of attention-related function between the SS and MS groups was analyzed
using Fisher’s non-parametric permutations test for continuous variables, which was also
used to analyze differences between diagnosed and undiagnosed attention problems in
each group. Mean age was adjusted for by analysis of covariance. Comparisons of
attention-related function with normative data included in the Conner CPT 3 test were
performed using the Wilcoxon signed rank test.
Correlations between attention and IQ-related variables and age were determined by
Pearson’s correlation coefficient.

Results
Patients
Patients (n = 106) were extracted from The Gothenburg Craniofacial Registry. Nine
patients were no longer living in the Västra Götaland or Halland region and were,
therefore, excluded. Eleven patients with sutures other than the sagittal or metopic suture
were excluded. Another six patients were excluded either due to language barrier (n = 1),
not having undergone surgery (n = 1), and having had secondary synostosis (n = 4).
Eighty patients and their parents were informed of the study, with ten families declining
to participate, and another five families unable to be reached by letter or telephone.
Ultimately, 65 families agreed to participate. Four families did not appear at the time
that their visit was planned, which resulted in 61 participating children, all of whom had
been surgically treated for sagittal (n = 38) or metopic (n = 23) synostosis. The mean ages
were 11.4 ± 2.4 years (range: 8–15 years) for sagittal synostosis and 10.0 ± 2.1 years (range
8–15 years) for metopic synostosis.
The mean ages at surgery were 275.2 ± 297.1 days (range: 91–1484 days) for sagittal
synostosis and 180.9 ± 88.9 (range 84–390 days) for metopic synostosis. The surgical
methods for sagittal synostosis included pi-plasty (n = 16, 42.1%), craniotomy combined
with springs (n = 21, 55.3%) and barrel-stave osteotomies (n = 1, 2.6%). For metopic
synostosis the surgical methods included a fronto-orbital reshaping in combination with
either with bone graft (n = 8, 34.8%) or a spring (n = 15, 65.2%).
Four of the patients (6.6%) were born prematurely, and 17 (27.9%) had an additional
diagnosis or disease, such as heart disease, asthma/allergy, migraine, metabolic disease, and/
or neuropsychiatric diagnosis. Eight (13.1%) patients received medication for medical
conditions but only one received medication specifically for an attention-related diagnosis
(Supplement 1).

Attrition analysis
All patients living in Västra Götaland or Halland region were included in the study,
which minimized the risk of selection bias. The response rate was 76.3%, with no
 CHILD NEUROPSYCHOLOGY 5

significant difference observed between the responding and non-responding groups in

regard to any of the background variables (Table 1).

The SS and MS groups

The SS group showed a significantly higher mean age than the MS group (p < 0.05). There
was a significant correlation between age and outcome and therefore the age difference
was adjusted for in subsequent comparisons of attention-related function
(Supplement 1).

Attention function associated with SS and MS

The SS group preformed significantly better at HRT as compared with the MS group
(p < 0.05). There were no other differences between the two groups (Table 2). However,
comparison of the SS and MS groups with the norms revealed several significant
differences. The SS group displayed worse response style, detectability, omissions, com-
missions, perseverations, HRT-SD, HRT-iC (p < 0.01 for all) and variability (p < 0.05)
The MS group displayed significantly worse detectability, HRT-SD, variability
(p < 0.01 for all) and commissions, perseverations, and HRT-iC (p < 0.05 for all)
(Table 3).

Table 1. Attrition analysis.

Non-responding Responding
Variable (n = 19) (n = 61) p
Gender
Female 6 (31.6%) 18 (29.5%)
Male 13 (68.4%) 43 (70.5%) 1.00
Age (y) 11.3 (2.2) 10.9 (2.4) 0.58
11.0 (8.0; 15.0) 10.0 (7.0; 15.0)
n = 19 n = 61
Type of craniosynostosis
Sagittal 12 (63.2%) 38 (62.3%)
Metopic 7 (36.8%) 23 (37.7%) 1.00
Surgery method
Pi-plasty 2 (10.5%) 16 (26.2%)
Craniotomy combined with springs 10 (52.6%) 23 (37.7%)
Fronto-orbital reshaping with bone graft 4 (21.1%) 8 (13.1%)
Fronto-orbital reshaping with spring 3 (15.8%) 13 (21.3%)
Barrel-stave osteotomy 0 (0.0%) 1 (1.6%) 0.48
Age at surgery (days) 184.6 (117.9) 239.7 (243.8) 0.36
138.0 (94.0; 583.0) 152.0 (84.0; 1484.0)
n = 19 n = 61
Number of surgeries for craniosynostosis
1 4 (21.1%) 25 (41.0%)
2 15 (78.9%) 36 (59.0%)
Born premature
Yes 3 (15.8%) 4 (6.6%)
No 16 (84.2%) 57 (93.4%) 0.42
For categorical variables n (%) is presented.
For continuous variables Mean (SD)/Median (Min; Max)/n = is presented.
For comparison between groups Fisher´s Exact test (lowest 1-sided p-value multiplied by 2) was used for dichotomous
variables and Chi Square test was used for non-ordered categorical variables and the Fisher´s Non Parametric
Permutation Test was used for continuous variables.
 6

Table 2. Connors CPT 3: comparison of attention-related problems between the SS and MS groups.
Sagittal (n = 38) Metopic (n = 23)
Mean (SD) Mean (SD)
Median (Min; Max) Median (Min; Max) Adjusted Difference between groups Effect
Variable n= n= p-value p-value* Adjusted Means (95% CI) Size
C: response style 52.5 (6.0) 51.7 (9.5) 0.70 0.90 0.260 (−3.907; 4.426) 0.105
52 (39; 68) 49 (35; 81)
M. KLJAJIĆ ET AL.

n = 38 n = 23
Detectability: ability to differentiate non-targets (X) from targets 56.8 (8.8) 55.6 (8.3) 0.61 0.24 2.75 (−1.90; 7.40) 0.139
59 (30; 69) 59 (38; 67)
n = 38 n = 23
Omissions: failure to respond to targets 56.5 (10.2) 54.9 (10.8) 0.56 0.42 2.37 (−3.43; 8.18) 0.156
55 (42; 83) 53 (41; 78)
n = 38 n = 23
Commissions: response to non-targets 54.3 (7.8) 54.4 (8.8) 0.96 0.48 1.55 (−2.80; 5.89) −0.016
56 (34; 66) 57 (31; 64)
n = 38 n = 23
Perseveration: random or anticipatory responses 58.9 (13.8) 56.2 (10.4) 0.43 0.31 3.61 (−3.42; 10.64) 0.216
54 (44; 90) 53 (44; 82)
n = 38 n = 23
HRT: mean response speed of correct responses throughout the test 49.5 (7.9) 53.9 (8.2) 0.041 0.049 −4.51 (−8.99; −0.03) −0.555
48 (36; 64) 52 (43; 74)
n = 38 n = 23
HRT-SD: consistency in response speed consistency throughout the test 56.6 (13.0) 57.0 (8.0) 0.89 0.64 1.46 (−4.70; 7.61) −0.039
55.5 (39; 90) 58 (44; 80)
n = 38 n = 23
Variability: consistency in response speed consistency within the respondent in relation to the HRT-SD 56.1 (13.3) 55.0 (8.1) 0.74 0.39 2.77 (−3.58; 9.12) 0.091
54 (38; 86) 55 (41; 77)
n = 38 n = 23
HRT-BC: change in the mean response speed across blocks 48.6 (9.7) 53.3 (10.6) 0.081 0.097 −4.72 (−10.34; 0.89) −0.473
48.5 (24; 72) 52 (35; 83)
n = 38 n = 23
HRT-iC: change in the mean response speed at various inter-stimulus intervals 55.2 (9.1) 53.8 (9.7) 0.58 0.29 2.74 (−2.38; 7.85) 0.153
55 (36; 79) 53 (34; 71)
n = 38 n = 23
For continuous variables Mean (SD)/Median (Min; Max)/n = is presented.
For comparison between groups the Fisher´s Non Parametric Permutation Test was used for continuous variables.
*Adjusting for age using Analysis of Covariance (ANCOVA).
Effect Size is Difference in Mean/Pooled SD.
Table 3. Connors CPT 3: comparison of attention-related problems between SS and norms and MS and norms..
Sagittal (n = 38) Metopic (n = 23)
Mean (SD) Mean (SD)
Median (Min; Max) Median (Min; Max)
Variable n= p-value within group Effect Size n= p-value within group Effect Size
C Response style (z-score) 0.253 (0.601) 0.0086 0.420 0.174 (0.945) 0.50 0.184
0.200 (−1.100; 1.800) -0.100 (−1.500; 3.100)
n = 38 n = 23
Detectability (z-score) 0.676 (0.883) <.0001 0.766 0.557 (0.829) 0.0047 0.671
0.900 (−2.000; 1.900) 0.900 (−1.200; 1.700)
n = 38 n = 23
Omissions (z-score) 0.650 (1.023) 0.0004 0.636 0.487 (1.076) 0.12 0.453
0.500 (−0.800; 3.300) 0.300 (−0.900; 2.800)
n = 38 n = 23
Commissions (z-score) 0.426 (0.781) 0.0013 0.546 0.439 (0.876) 0.014 0.501
0.600 (−1.600; 1.600) 0.700 (−1.900; 1.400)
n = 38 n = 23
Perseverations (z-score) 0.889 (1.375) 0.0007 0.647 0.617 (1.044) 0.012 0.591
0.400 (−0.600; 4.000) 0.300 (−0.600; 3.200)
n = 38 n = 23
HRT (z-score) −0.053 (0.790) 0.65 −0.067 0.391 (0.818) 0.066 0.478
-0.200 (−1.400; 1.400) 0.200 (−0.700; 2.400)
n = 38 n = 23
HRTSD (z-score) 0.661 (1.298) 0.0077 0.509 0.704 (0.799) <.0001 0.882
0.550 (−1.100; 4.000) 0.800 (−0.600; 3.000)
n = 38 n = 23
Variability (z-score) 0.611 (1.332) 0.018 0.458 0.504 (0.805) 0.0038 0.626
0.400 (−1.200; 3.600) 0.500 (−0.900; 2.700)
n = 38 n = 23
HRT block Change (z-score) −0.139 (0.967) 0.41 −0.144 0.335 (1.058) 0.19 0.316
-0.150 (−2.600; 2.200) 0.200 (−1.500; 3.300)
n = 38 n = 23
HRT isi Change (z-score) 0.521 (0.914) 0.0012 0.570 0.378 (0.969) 0.045 0.391
0.500 (−1.400; 2.900) 0.300 (−1.600; 2.100)
n = 38 n = 23
CHILD NEUROPSYCHOLOGY

For continuous variables Mean (SD)/Median (Min; Max)/n = is presented.

For comparison within groups the Wilcoxon Signed Rank test was used.
Effect Size is Mean/SD.
7
8 M. KLJAJIĆ ET AL.

Patients with attention problems

Comparison between patients diagnosed with attention-related problems and those undiag-
nosed showed a significant difference, and large effect size (−0.934), in perseveration
(p < 0.05), with the diagnosed group showing higher scores for random responses (Table 4).
Background variables in Supplement 2.

Timing, surgical technique and attention in sagittal synostosis

Comparison of patients with sagittal synostosis operated with two different surgical
methods, i.e. craniotomy combined with springs before 6 months of age (n = 21) and pi-
plasty after 6 months of age (n = 16) did not reveal any differences in sustained attention
or vigilance (Table 5).
Background variables in Supplement 3.

Correlations between attention-related function and general cognitive function

Perseveration, HRT-SD, and variability were significantly correlated with both full-scale
IQ (FSIQ) and verbal-comprehension IQ (VCIQ), although these correlations were
negative and accompanied by small effects (Table 6).

Discussion
These results were obtained from a specific test of sustained attention and vigilance
applied to a group of children with non-syndromic CS. The main finding of the study was
that children treated for SS or MS showed several significant impairments of attention
when compared with norms according to the Conner CPT 3 test. The SS group showed
worse response style, detectability, omissions, commissions, perseverations, HRT-SD,
HRT-iC, and variability, and the MS group showed significantly worse detectability,
commissions, perseverations, HRT-SD, variability, and HRT-iC relative to norms. These
results suggested the presence of various attention-related problems, including inatten-
tiveness, impulsivity, and lack of sustained attention and vigilance. However, despite the
significance of the differences indicating attention-related issues in the patient cohort, the
differences were still within one standard deviation.
Previous studies reported an association between both SS and MS and neuropsycho-
logical impairments (Collett et al., 2017; Speltz et al., 2004). Specific testing of attention
combined with comparison of different isolated synostoses, as in the present study, is
however rare (Collett et al., 2017).
In the present study, we found only one difference between the SS and MS groups,
with the SS group showing a significantly better HRT-SD, which is only one of several
measures of inattentiveness. However, as noted, both groups displayed several attention-
related impairments as compared with norms.
Our cohort included also children previously diagnosed with attention-related pro-
blems, including ADHD and problems with executive function and inattentiveness.
Comparison between the diagnosed and undiagnosed groups revealed a single significant
difference involving worse perseveration in the diagnosed group, indicating that their
Table 4. Connors CPT 3: undiagnosed patients and those diagnosed with attention-related problems. .
Undiagnosed Attention-related diagnosis Difference between groups Effect
Variable (n = 56) (n = 5) p-value Mean (95% CI) Size
C: response style 52.5 (7.5) 49.6 (7.2) 0.40 2.86 (−3.63; 10.48) 0.384
52.0 (35.0; 81.0) 50.0 (41.0; 58.0)
n = 56 n=5
Detectability: ability to differentiate non-targets (X) from targets 55.9 (8.3) 61.0 (11.8) 0.21 −5.11 (−13.94; 2.17) −0.598
59.0 (30.0; 68.0) 66.0 (41.0; 69.0)
n = 56 n=5
Omissions: failure to respond to targets 55.4 (9.7) 61.0 (16.5) 0.26 −5.57 (−14.96; 4.90) −0.539
53.0 (42.0; 83.0) 65.0 (41.0; 82.0)
n = 56 n=5
Commissions: response to non-targets 53.9 (8.1) 59.0 (8.0) 0.19 −5.11 (−13.19; 1.75) −0.634
56.0 (31.0; 66.0) 61.0 (45.0; 65.0)
n = 56 n=5
Perseveration: random or anticipatory responses 56.9 (12.1) 68.4 (14.3) 0.043 −11.5 (−21.6; 1.3) −0.934
53.0 (44.0; 90.0) 69.0 (50.0; 87.0)
n = 56 n=5
HRT: mean response speed of correct responses throughout the test 51.2 (7.9) 50.2 (12.2) 0.80 1.03 (−6.49; 9.31) 0.124
51.0 (36.0; 74.0) 45.0 (36.0; 64.0)
n = 56 n=5
HRT-SD: consistency in response speed consistency throughout the test 56.1 (10.5) 64.2 (17.9) 0.12 −8.09 (−17.96; 3.54) −0.726
56.0 (39.0; 88.0) 59.0 (45.0; 90.0)
n = 56 n=5
Variability: consistency in response speed consistency within the respondent in relation to the HRT-SD 55.2 (11.2) 61.2 (15.1) 0.28 −5.99 (−15.79; 5.96) −0.519
54.0 (38.0; 86.0) 59.0 (47.0; 86.0)
n = 56 n=5
HRT-BC: change in the mean response speed across blocks 50.5 (10.1) 49.6 (13.0) 0.87 0.864 (−8.653; 10.882) 0.084
50.5 (24.0; 83.0) 51.0 (33.0; 66.0)
n = 56 n=5
HRT-iC: change in the mean response speed at various inter-stimulus intervals 54.2 (9.4) 59.6 (7.8) 0.22 −5.37 (−13.88; 3.34) −0.580
53.0 (34.0; 79.0) 58.0 (50.0; 68.0)
n = 56 n=5
For continuous variables Mean (SD)/Median (Min; Max)/n = is presented.
For comparison between groups the Fisher´s Non Parametric Permutation test was used for continuous variables. The confidence interval for then mean difference between groups is based on
CHILD NEUROPSYCHOLOGY

Fishers non-parametric permutation test.

Effect Size is Difference in Mean/Pooled SD.
9
 10

Table 5. Comparisons between surgical techniques for sagittal synostosis and attention.
Craniotomy combined with Difference between
springs Pi-plasty groups Effect
Variable (n = 21) (n = 16) p-value Mean (95% CI) Size
C: response style 52.2 (5.2) 53.1 (7.2) 0.67 0.887 (−3.259; 5.006) 0.145
52.0 (42.0; 63.0) 53.0 (39.0; 68.0)
n = 21 n = 16
M. KLJAJIĆ ET AL.

Detectability: ability to differentiate non-targets (X) from targets 56.8 (10.2) 56.4 (7.2) 0.91 −0.372 (−6.364; 5.753) −0.041
59.0 (30.0; 69.0) 57.0 (45.0; 66.0)
n = 21 n = 16
Omissions: failure to respond to targets 56.4 (10.2) 56.3 (10.8) 0.98 −0.116 (−7.296; 6.894) −0.011
56.0 (43.0; 82.0) 53.5 (42.0; 83.0)
n = 21 n = 16
Commissions: response to non-targets 54.3 (8.5) 53.8 (7.2) 0.87 −0.473 (−5.746; 4.894) −0.060
56.0 (34.0; 66.0) 53.5 (44.0; 66.0)
n = 21 n = 16
Perseveration: random or anticipatory responses 57.6 (12.5) 61.0 (15.8) 0.48 3.38 (−6.18; 12.76) 0.242
56.0 (44.0; 87.0) 52.5 (45.0; 90.0)
n = 21 n = 16
HRT: mean response speed of correct responses throughout the test 48.9 (7.5) 50.6 (8.6) 0.52 1.72 (−3.72; 7.09) 0.215
48.0 (36.0; 64.0) 51.5 (36.0; 62.0)
n = 21 n = 16
HRT-SD: consistency in response speed consistency throughout the test 55.5 (14.4) 58.0 (11.6) 0.59 2.48 (−6.59; 11.26) 0.186
52.0 (41.0; 90.0) 56.0 (39.0; 80.0)
n = 21 n = 16
Variability: consistency in response speed consistency within the respondent in relation to the 53.7 (13.1) 59.0 (13.8) 0.25 5.29 (−3.87; 14.21) 0.394
HRT-SD 52.0 (38.0; 86.0) 57.5 (40.0; 86.0)
n = 21 n = 16
HRT-BC: change in the mean response speed across blocks 49.1 (7.1) 48.0 (12.7) 0.76 −1.10 (−7.82; 5.58) −0.110
51.0 (33.0; 66.0) 48.5 (24.0; 72.0)
n = 21 n = 16
HRT-iC: change in the mean response speed at various inter-stimulus intervals 53.3 (9.1) 57.8 (9.1) 0.15 4.46 (−1.71; 10.59) 0.489
50.0 (36.0; 69.0) 56.0 (45.0; 79.0)
n = 21 n = 16
For continuous variables Mean (SD)/Median (Min; Max)/n = is presented.
For comparison between groups the Fisher´s Non Parametric Permutation Test was used for continuous variables. The confidence interval for then mean difference between groups is based on
Fishers non-parametric permutation test.
Effect Size is Difference in Mean/Pooled SD.
Table 6. Correlations between attention-, IQ-related variables and age. .
Variable FSIQ VCIQ PRIQ WMIQ PSIQ Mean age
C: response style −0.16 −0.17 −0.24 0.02 −0.02 0.12
p = 0.21 p = 0.20 p = 0.068 p = 0.90 p = 0.86 p = 0.36
Detectability: ability to differentiate non-targets (X) from targets −0.13 −0.10 −0.09 0.01 −0.19 −0.24
p = 0.32 p = 0.46 p = 0.48 p = 0.95 p = 0.14 p = 0.060
Omissions: failure to respond to targets −0.20 −0.21 −0.23 0.07 −0.11 −0.08
p = 0.13 p = 0.10 p = 0.073 p = 0.62 p = 0.40 p = 0.54
Commissions: response to non-targets −0.04 −0.03 0.03 0.04 −0.16 −0.30
p = 0.77 p = 0.82 p = 0.82 p = 0.74 p = 0.23 p = 0.018
Perseveration: random or anticipatory responses −0.26 −0.28 −0.17 −0.09 −0.25 −0.07
p = 0.040 p = 0.030 p = 0.18 p = 0.48 p = 0.055 p = 0.59
HRT: mean response speed of correct responses throughout the test −0.18 −0.16 −0.13 −0.08 −0.21 −0.07
p = 0.16 p = 0.20 p = 0.31 p = 0.55 p = 0.11 p = 0.60
HRT-SD: consistency in response speed consistency throughout the test −0.30 −0.35 −0.21 −0.13 −0.20 −0.25
p = 0.017 p = 0.0051 p = 0.10 p = 0.32 p = 0.11 p = 0.052
Variability: consistency in response speed consistency within the respondent in relation to the HRT-SD −0.30 −0.31 −0.22 −0.21 −0.17 −0.20
p = 0.021 p = 0.015 p = 0.091 p = 0.11 p = 0.18 p = 0.12
HRT-BC: change in the mean response speed across blocks 0.01 0.05 0.02 0.01 −0.09 −0.07
p = 0.96 p = 0.73 p = 0.90 p = 0.91 p = 0.50 p = 0.58
HRT-iC: change in the mean response speed at various inter-stimulus intervals −0.08 −0.15 0.02 0.06 −0.11 −0.18
p = 0.52 p = 0.25 p = 0.91 p = 0.63 p = 0.38 p = 0.16
Data represent Pearson’s correlation coefficients.
FSIQ = full-scale IQ; IQ = intelligence quotient; PRIQ = perceptual-reasoning IQ; PSIQ = processing-speed IQ; VCIQ = verbal-comprehension IQ; WMIQ = working-memory IQ.
CHILD NEUROPSYCHOLOGY
11
12 M. KLJAJIĆ ET AL.

responses during the test were more random than anticipated. This might be indicative of
the sensitivity of the Conner CPT 3 test and its ability to detect deviations in attention
performance. For several other variables we noted medium to large effect sizes but the
low number of cases might explain that the differences were insignificant. Furthermore,
we did not interfere with medication aiming at ameliorating the effect of ADHD.
The effect of surgery on neurodevelopmental outcome is unclear (Mandela, Bellew,
Chumas, & Nash, 2019). In SS it has been suggested that early surgery and more extensive
surgery are favorable for neurodevelopmental outcome (Hashim et al., 2014; Patel et al.,
2014). In the present study we compared the outcome regarding attention for two
distinctly different surgical methods for correction of SS, i.e. craniotomy combined
with springs before 6 months of age and the significantly more extensive pi-plasty
performed after 6 months of age. These methods correct skull shape equally well
(Fischer et al., 2016). Irrespective of surgical method, the children performed equally
well regarding sustained attention and vigilance.
Previous studies assessed attention problems using questionnaires, with results reflective
of perceived problems rather than measured problems (Speltz et al., 2016; van der Vlugt
et al., 2012). Other studies used tests of attention with complementary testing of IQ (Collett
et al., 2017). In the present study, the assessment was performed using a computerized
continuous performance test and included additional background data concerning the
general cognitive function of each child. There was a small difference between SS and MS
regarding working memory. However, there was no significant correlation between work-
ing memory and any of the attention variables. For other domains of cognitive function
there were correlations with attention but these domains were evenly distributed between
the SS and MS groups. Therefore, no adjustment for working memory was made.
The response rate in the study was high (76.3%). Moreover, the Gothenburg
Craniofacial Registry enabled attrition analysis, which showed no differences between
responding and non-responding groups.
This study has some limitations. First, the study group was small; however, only
a small number of patients was not included in the study cohort due to the exclusion
criteria, and the two groups were comparable in terms of child and family variables,
thereby minimizing the risk of selection bias. Second, there was no control group used in
the study. Comparisons were performed using US normative data included in the Conner
CPT 3 test, since no Swedish norms are available. Third, there was no complete
information about the socioeconomic status of the families. Educational level, but not
family income, was known.

Conclusion
Children operated for sagittal and metopic CS display several shortcomings regarding
sustained attention and vigilance. However, the differences as compared with the nor-
mative data included in the Conner CPT 3 test used in this study were minimal and likely
of no clinical relevance.

Disclosure statement
No potential conflict of interest was reported by the authors.
 CHILD NEUROPSYCHOLOGY 13

Funding
This work was supported by the Swedish state under the agreement between the government and
the county councils, the ALF-agreement [ALFGBG-716621].

References
Austerman, J. (2015). ADHD and behavioral disorders: Assessment, management, and an update
from DSM-5. Cleveland Clinic Journal of Medicine, 82(11 Suppl 1), S2–S7.
Bellew, M., & Chumas, P. (2015). Long-term developmental follow-up in children with nonsyn-
dromic craniosynostosis. Journal of Neurosurgery: Pediatrics, 16(4), 445–451.
Bellew, M., Liddington, M., Chumas, P., & Russell, J. (2011). Preoperative and postoperative
developmental attainment in patients with sagittal synostosis: 5-year follow-up. Journal of
Neurosurgery: Pediatrics, 7(2), 121–126.
Berg, D. H. (2008). Working memory and arithmetic calculation in children: The contributory
roles of processing speed, short-term memory, and reading. Journal of Experimental Child
Psychology, 99(4), 288–308.
Berger, I., Slobodin, O., & Cassuto, H. (2017). Usefulness and validity of continuous performance
tests in the diagnosis of attention-deficits hyperactivity disorder children. Archives of Clinical
Neuropsychology, 32(1), 81–93.
Brydges, C. R., Ozolnieks, K. L., & Roberts, G. (2017). Working memory–Not processing speed–
Mediates fluid intelligence deficits associated with attention deficit/hyperactivity disorder
symptoms. Journal of Neuropsychology, 11(3), 362–377.
Chieffo, D., Tamburrini, G., Massimi, L., Di Giovanni, S., Giansanti, C., Caldarelli, M., & Di
Rocco, C. (2010). Long-term neuropsychological development in single-suture craniosynostosis
treated early. Journal of Neurosurgery: Pediatrics, 5(3), 232–237.
Collett, B. R., Kapp-Simon, K. A., Wallace, E., Cradock, M. M., Buono, L., & Speltz, M. L. (2017).
Attention and executive function in children with and without single-suture craniosynostosis.
Child Neuropsychology, 23(1), 83–98.
Connors, K. (2014). Connors continuous performance test, 3rd edition (Connors CPT 3), Connors
continuous auditory test of attention (Connors CATA). Technical Manual.
Fischer, S., Maltese, G., Tarnow, P., Wikberg, E., Bernhardt, P., & Kölby, L. (2016). Comparison of
intracranial volume and cephalic index after correction of sagittal synostosis with
spring-assisted surgery or pi-plasty. Journal of Craniofacial Surgery, 27(2), 410–413.
Hashim, P. W., Patel, A., Yang, J. F., Travieso, R., Terner, J., Losee, J. E., . . . Persing, J. A. (2014).
The effects of whole-vault cranioplasty versus strip craniectomy on long-term neuropsycholo-
gical outcomes in sagittal craniosynostosis. Plastic and Reconstructive Surgery, 134(3), 491–501.
Kapp-Simon, K. A., Leroux, B., Cunningham, M., & Speltz, M. L. (2005). Multi-site study of infants
with single-suture craniosynostosis: Preliminary report of presurgery development. The Cleft
Palate-Craniofacial Journal: Official Publication of the American Cleft Palate-Craniofacial
Association, 42(4), 377–384.
Kapp-Simon, K. A., Speltz, M. L., Cunningham, M. L., Patel, P. K., & Tomita, T. (2007).
Neurodevelopment of children with single suture craniosynostosis: A review. Child’s Nervous
System: ChNS: Official Journal of the International Society for Pediatric Neurosurgery, 23(3),
269–281.
Kapp-Simon, K. A., Wallace, E., Collett, B. R., Cradock, M. M., Crerand, C. E., & Speltz, M. L.
(2016). Language, learning, and memory in children with and without single-suture
craniosynostosis. Journal of Neurosurgery: Pediatrics, 17(5), 578–588.
Kljajić, M., Maltese, G., Tarnow, P., Sand, P., & Kölby, L. (2019). The cognitive profile of children
with non-syndromic craniosynostosis. Plastic and Reconstructive Surgery, 143(5), 1037e–1052e.
Lundervold, A. J., Stickert, M., Hysing, M., Sorensen, L., Gillberg, C., & Posserud, M. B. (2016).
Attention deficits in children with combined autism and ADHD: A CPT Study. Journal of
Attention Disorders, 20(7), 599–609.
14 M. KLJAJIĆ ET AL.

Magge, S. N., Westerveld, M., Pruzinsky, T., & Persing, J. A. (2002). Long-term neuropsychological
effects of sagittal craniosynostosis on child development. The Journal of Craniofacial Surgery, 13
(1), 99–104.
Mandela, R., Bellew, M., Chumas, P., & Nash, H. (2019). Impact of surgery timing for craniosynostosis
on neurodevelopmental outcomes: A systematic review. Journal of Neurosurgery, 23(4), 442–454.
Mathijssen, I. M. J. (2015). Guideline for care of patients with the diagnoses of craniosynostosis:
Working group on craniosynostosis. The Journal of Craniofacial Surgery, 26(6), 1735–1807.
Memoria, C. M., Muela, H. C. S., Moraes, N. C., Costa-Hong, V. A., Machado, M. F., Nitrini, R., . . .
Yassuda, M. S. (2018). Applicability of the test of variables of attention—T.O.V.A in Brazilian
adults. Dementia & Neuropsychologia, 12(4), 394–401.
Osborn, A. J., Roberts, R. M., Mathias, J. L., Anderson, P. J., & Flapper, W. J. (2019). Cognitive,
behavioral and psychological functioning in children with metopic synostosis: A meta-analysis
examining the impact of surgical status. Child Neuropsychology, 25(2), 263–277.
Patel, A., Yang, J. F., Hashim, P. W., Travieso, R., Terner, J., Mayes, L. C., . . . Persing, J. A. (2014).
The impact of age at surgery on long-term neuropsychological outcomes in sagittal
craniosynostosis. Plastic and Reconstructive Surgery, 134(4), 608e–617e.
Perez-Olmos, I., & Ibanez-Pinilla, M. (2014). Night shifts, sleep deprivation, and attention
performance in medical students. International Journal of Medical Education, 5, 56–62.
Speltz, M. L., Collett, B. R., Wallace, E. R., & Kapp-Simon, K. (2016). Behavioral adjustment of
school-age children with and without single-suture craniosynostosis. Plastic and Reconstructive
Surgery, 138(2), 435–445.
Speltz, M. L., Collett, B. R., Wallace, E. R., Starr, J. R., Cradock, M. M., Buono, L., . . . Kapp-Simon,
K. (2015). Intellectual and academic functioning of school-age children with single-suture
craniosynostosis. Pediatrics, 135(3), e615–e623.
Speltz, M. L., Kapp-Simon, K. A., Cunningham, M., Marsh, J., & Dawson, G. (2004). Single-suture
craniosynostosis: A review of neurobehavioral research and theory. The Journal of Pediatric
Psychology, 29(8), 651–668.
van der Vlugt, J. J., van der Meulen, J. J., Creemers, H. E., Verhulst, F. C., Hovius, S. E., &
Okkerse, J. M. (2012). Cognitive and behavioral functioning in 82 patients with trigonocephaly.
Plastic and Reconstructive Surgery, 130(4), 885–893.
Subcommittee on Attention-Deficit/Hyperactivity Disorder; Steering Committee on Quality
Improvement and Management, Wolraich, M., Brown, L., Brown, R. T., DuPaul, G.,
Earls, M., Feldman, H. M., . . . Visser, S. (2011). ADHD: Clinical practice guideline for the
diagnosis, evaluation, and treatment of attention-deficit/hyperactivity disorder in children and
adolescents. Pediatrics, 128(5), 1007–1022.