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Review article
Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, PR China
Department of Radiation Oncology, University of Texas Southwestern Medical Center, Dallas, TX, USA
c
Department of Psychiatry, West China Hospital of Sichuan University, Chengdu, PR China
b
a r t i c l e
i n f o
Article history:
Received 9 January 2016
Received in revised form 18 July 2016
Accepted 19 July 2016
Available online 20 July 2016
Keywords:
Meta-analysis
Attention-decit/hyperactivity disorder
Diffusion tensor imaging
Tract-based spatial statistics
Fractional anisotropy
Seed-based d mapping
a b s t r a c t
Diffusion tensor imaging (DTI) studies that use tract-based spatial statistics (TBSS) have demonstrated
the microstructural abnormalities of white matter (WM) in patients with attention-decit/hyperactivity
disorder (ADHD); however, robust conclusions have not yet been drawn. The present study integrated
the ndings of previous TBSS studies to determine the most consistent WM alterations in ADHD via a
narrative review and meta-analysis. The literature search was conducted through October 2015 to identify
TBSS studies that compared fractional anisotropy (FA) between ADHD patients and healthy controls.
FA reductions were identied in the splenium of the corpus callosum (CC) that extended to the right
cingulum, right sagittal stratum, and left tapetum. The rst two clusters retained signicance in the
sensitivity analysis and in all subgroup analyses. The FA reduction in the CC splenium was negatively
associated with the mean age of the ADHD group. We hypothesize that, in addition to the fronto-striatalcerebellar circuit, the disturbed WM matter tracts that integrate the bilateral hemispheres and posteriorbrain circuitries play a crucial role in the pathophysiology of ADHD.
2016 Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
4.
5.
6.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 839
Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 839
2.1.
Study selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 839
2.2.
Quality assessment checklist and narrative review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 840
2.3.
SDM meta-analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 840
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 840
3.1.
Characteristics of the studies included in the meta-analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 840
3.2.
Quality assessment and narrative review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 842
3.3.
SDM meta-analysis results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 843
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 843
Limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 845
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 846
Conicts of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 846
Corresponding authors at: Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, No. 37 Guo Xue Xiang, Chengdu
610041, PR China.
E-mail addresses: julianahuang@163.com (X. Huang), qiyonggong@hmrrc.org.cn (Q. Gong).
1
These authors have contributed equally to this study.
http://dx.doi.org/10.1016/j.neubiorev.2016.07.022
0149-7634/ 2016 Elsevier Ltd. All rights reserved.
839
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 846
Appendix A.
Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 846
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 846
1. Introduction
Attention-decit/hyperactivity disorder (ADHD) is a commonly diagnosed neurodevelopmental disorder that begins during
childhood and is characterized by age-inappropriate levels of
hyperactivity, impulsivity and inattention (American Psychiatric
Association, 2013). The worldwide prevalence of ADHD is over 5%
among school-age children (Polanczyk et al., 2007), and 65% of
those cases continue into adulthood (Faraone et al., 2006). Magnetic resonance imaging (MRI) is extensively used in research to
elucidate the pathogenesis of ADHD and has primarily embraced a
neuronal network model of the fronto-striatal-cerebellar circuit,
which can explain some of the disturbances in patients. Recent
evidence has additionally suggested anomalies in a number of different networks involving large-scale brain regions, such as the
interhemispheric pathways and the occipital and temporal lobes
(Castellanos and Proal, 2012). In morphometric studies, consistent
reductions have been reported in total cerebral white matter (WM)
volume, all four lobes and specic structures such as the corpus
callosum (CC) (Krain and Castellanos, 2006; McAlonan et al., 2007;
Seidman et al., 2005). One review even observed a more predominant volume reduction of WM than gray matter (GM) in patients
with ADHD (Castellanos et al., 2002). The above evidence demonstrates that WM abnormalities play an important role in ADHD
pathophysiology.
Compared with macrostructural MRI for morphometric
changes, diffusion tensor imaging (DTI) enables researchers
to examine WM properties at a microstructural level (Basser,
1995). Fractional anisotropy (FA) is the most commonly used DTI
parameter for investigating the anisotropy that quanties the
directionality of diffusion. FA is regarded as a relatively nonspecic
biomarker for brain WM microstructural architecture and neuropathology (Alexander et al., 2007). Other diffusion parameters
often used in DTI studies include mean diffusivity (MD), which
reects the magnitude of diffusion in WM pathways; axial diffusivity (AD) and radial diffusivity (RD). The latter two parameters
provide complementary information to help understand the FA
or MD changes, reecting the diffusion parallel with and perpendicular to the axon, respectively. Concerning the approaches used
to analyze parameters, whole-brain analyses such as voxel-based
analysis (VBA) and tract-based spatial statistics (TBSS) provide
better comparability across studies than region-of-interest (ROI)
analyses because they overcome the bias of region-placement
preference and the absence of meaningful voxels outside of the
selected regions. In the past, whole-brain DTI studies of ADHD have
successfully identied increased and decreased FA in various brain
regions, including the prefrontal WM, temporal WM, cingulum
bundle, CC, and cerebellum (Krain and Castellanos, 2006; Valera
et al., 2007).
To resolve the inconsistency across different studies, van Ewijk
and colleagues conducted a literature review of pertinent DTI
studies on ADHD and a coordinate-based meta-analysis of nine
whole-brain studies (seven VBA and two TBSS studies) in 2011 (van
Ewijk et al., 2012). Although it was useful at the time, this study
has limitations. For example, although VBA and TBSS both explore
whole-brain WM alterations, they have inherent methodical differences that make combined meta-analysis problematic. TBSS was
specically developed to analyze diffusion data (Smith et al., 2006),
and it restricts analysis to the center of the major WM tracts (in
contrast with VBA, which analyzes all WM regions). Many recent
studies have used this approach and, in fact, there have been more
TBSS studies published than VBA studies. Thus, it is possible and
timely to perform a meta-analysis based solely on TBSS studies.
Previous literature has demonstrated marked delays in cortical
maturation among children with ADHD compared with typically
developing controls (Shaw et al., 2007), although these ADHD
patients might progressively catch up with age (Nakao et al., 2011).
Moreover, the use of medication, especially methylphenidate,
might normalize structural WM and GM changes as well as the trajectory of cortical development in patients with ADHD (Schweren
et al., 2013). Much evidence also suggests the presence of a gender
effect in ADHD, especially in children and adolescents (Biederman
et al., 2002). The male-to-female ratio in youth with ADHD ranges
from 2:1 to 9:1 (Biederman et al., 2004), and clinical manifestations and cognitive impairments differ between genders (Gershon,
2002). Thus, developmental trajectory, medication use and gender are associated with the pathophysiology and disease process of
ADHD.
Given the above research, the current study sought to identify
the most prominent and replicable WM microstructural abnormalities based on TBSS studies of ADHD and review the ndings.
A meta-analysis was performed using seed-based d mapping
(SDM) software, which enables the results from individual studies
to be weighted and controlled for multiple moderators including demographics, clinical information and imaging factors. More
importantly, SDM considers null results in a meta-analysis, and
it has been successfully applied in other neuropsychiatric studies
using TBSS (Welton et al., 2015). In addition, a multiple regression analysis was applied to explore the potential effects of age,
medication use and gender on WM microstructural differences.
2. Methods
2.1. Study selection
Comprehensive online searches for pertinent literature were
performed using the PubMed, Web of Science, EMBASE, EBSCO,
Clinical Key and Science Direct databases. All of the included studies were peer-reviewed articles published before October 2015.
The key search terms were attention-decit hyperactivity disorder, ADHD or hyperkinetic; tract-based spatial statistical
or TBSS; diffusion tensor or DTI; and fractional anisotropy
or FA. Moreover, all of the review articles and their references
were manually searched. All of the yielded articles were assessed
for potential suitability, and the articles that met the following
inclusion criteria were included in the meta-analysis: (i) published
in English in a peer-reviewed journal, (ii) included participants
with a primary diagnosis of ADHD and a group of healthy controls, (iii) reported a TBSS comparison between patients with ADHD
and healthy controls, (iv) used signicance thresholds for data that
were either corrected for multiple comparisons or uncorrected
with spatial extent thresholds, and (v) reported the whole-brain
results of FA alterations in a stereotactic space using the threedimensional standard coordinates (Talairach or MNI) of group
changes. The corresponding authors of articles that did not report
whole-brain coordinates but were otherwise suitable for metaanalysis were contacted for additional information. Theoretical
studies and reviews were excluded. Studies that used multiple
independent patient samples were separately compared with same
840
Table 1
The characteristics of the ADHD studies included in the meta-analysis.
Study
Medicationa , %
Age, years
IQ
ADHD
HC
ADHD
HC
ADHD
HC
Silk
15 (15)
15 (15)
12.6 (2.4)
12.9 (2.6)
Nagel
20 (4)
20 (13)
8.31 (0.70)
8.05 (0.69)
PIQ: 104.9
(11.5) VIQ:
102.9 (14.7)
115.4 (12.9)
Chuang
12 (12)
14 (14)
14.8 (1.4)
15.7 (NA)
Cortese PER
15 (15)
47 (47)
41.8 (3.0)
Cortese REM
Bode
Cooper
van Ewijk
25 (25)
30 (21)
17 (17)
170 (115)
47 (47)
30 (22)
17 (17)
107 (52)
de Luis-Garca NT
de Luis-Garca UT
OConaill
Onnink
16 (16)
24 (24)
19 (17)
107 (41)
26 (26)
26 (26)
21 (16)
109 (47)
Study information
MRI Telsa
Directions
Statistical threshold
20
28
Corrected by NPT
106.5 (12.8)
15
20
Corrected by AlphaSim
99.3 (11.7)
102.4 (9.3)
91.7
1.5
na
Corrected by NPT
41.1 (3.0)
99.3 (13.0)
111.1 (14.3)
92
Corrected by TFCE
41.3 (2.6)
22.59 (0.76)
15.6 (1.3)
17.3 (3.3)
41.1 (3.0)
23.09 (0.64)
16.9 (1.2)
16.4 (3.1)
103.8 (13.1)
98.17 (18.22)
87.6 (9.8)
97.8 (14.7)
111.1 (14.3)
110.00 (22.48)
106.9 (7.6)
104.5 (13.7)
92
0
58.8
90.3
3
1.5
3
1.5
6
40
60
60
Corrected by TFCE
Corrected by NDMS
Corrected by TFCE
Corrected by TFCE
7.62 (1.36)
8.50 (1.1)
11.93 (1.33)
35.00 (10.30)
8.23 (1.53)
8.23 (1.53)
12.60 (1.29)
36.08 (10.97)
100.3 (18.2)
103.3 (13.3)
95.79 (16.97)
108.13 14.43
120.3 (14.5)
120.3 (14.5)
107.81 (13.08)
110.97 15.36
0
100
78.9
81
1.5
1.5
3
1.5
25
25
20
34
Corrected by TFCE
Corrected by TFCE
Uncorrected
Corrected by TFCE
Participants, n (males)
ACR: anterior corona radiata; ADHD: attention-decit/hyperactivity disorder; ATR: anterior thalamic radiation; B: bilateral; CG: cingulum; CST: corticospinal tract; EC: external capsule; FA: fractional anisotropy; HC: healthy
controls; ICP: inferior cerebellar peduncle; IC: internal capsule; IFOF: inferior fronto-occipital fasciculus; ILF: inferior longitudinal fasciculus; L: left; MCP: middle cerebellar peduncle; OR: optic radiation; PCR: posterior corona
radiata; PTR: posterior thalamic radiation; R: right; RIC: retrolenticular part of internal capsule; SCR: superior corona radiata; SLF: superior longitudinal fasciculus; SS: sagittal stratum; UF: uncinate fasciculus.
a
Indicates patients who received medication during scanning or had a past history of medication (but washed out before scanning); only those who were never medicated were excluded.
841
842
843
Fig. 2. Three clusters with decreased FA were identied in patients with ADHD compared with healthy controls: the splenium of the CC extending to the right cingulum,
the right SS, and the left CC tapetum.
844
Table 2
Regional differences in FA between patients with ADHD and healthy controls.
WM Tract
Voxels, n
SDM z value
p, uncorrected
CC splenium
363
16
34
28
2.111
Right SS
127
42
28
12
1.669
0.000007331
Left CC tapetum
30
32
32
1.097
0.000600994
CC: corpus callosum; FA: fractional anisotropy; MNI: Montreal Neurological Institute; SDM: Seed-based d mapping; SS: sagittal stratum; WM: white matter.
Fig. 3. The meta-regression results showing that the FA values of two subparts in the CC splenium were negatively associated with the mean age of patients with ADHD:
the anterior part (right, r = 0.338, permutation-derived p < 0.0001) and posterior part (left, r = 0.312, permutation-derived p < 0.0001). The effects sizes shown in the graphs
needed to create the plots were extracted. Larger dots indicate larger sample sizes.
which was suggested to indicate a familial liability for ADHD. Furthermore, as no tested tracts showed a signicant FA difference,
the authors suspected that MD might be a more sensitive biological marker for ADHD and/or that FA effects were more variable or
restricted to specic aspects of tracts that were missed by the tractography method. In contrast, van Ewijk and colleagues (van Ewijk
et al., 2014) found that subjects with ADHD showed decreased FA
and MD in non-overlapping areas in comparison with healthy controls. However, unaffected siblings resembled patients with regard
to decreased FA but had MD similar to that of controls. The authors
thus suggested that the FA reduction, but not the MD reduction, was
due to a familial vulnerability to ADHD. Such study discrepancies
in MD results may be related to methodological differences, as suggested by van Ewijk, or other unidentied factors to be identied
in future meta-analysis with adequate evidence of MD (if possible,
AD and RD should also be analyzed). Moreover, as these diffusion
parameters are subject to different interpretations among different
analyses, the combined use of essential indexes is recommended.
The CC is the largest WM bundle that connects the bilateral
cerebral hemispheres, transferring excitatory and inhibitory signals (McNally et al., 2010). The present study found decreased
FA in the splenium of the CC extending to the posterior portion of the right cingulum, thereby suggesting an interruption
in the inter-hemispheric communication of the posterior brain
within the limbic network. The splenium connects the bilateral
occipital, temporal and posterior parietal areas (Hofer and Frahm,
2006), inuencing the speed of visual information transmission
and dynamically distributing processing resources (Putnam et al.,
2010). Thus, the decits along the splenium pathway might be
related to the inattention, distractibility, and visual dysfunctions
observed among patients with ADHD. Moreover, because the CC
is the major bridge across the two hemispheres, its decits might
also disentangle the lateralization problems observed among those
with ADHD (Giedd et al., 2001). In healthy controls, there is an information transfer asymmetry between the two hemispheres, with
more rapid transfer from the right to left side than in the opposite
direction (Miller, 1996). Some researchers have found this normal
asymmetry to be altered in ADHD patients, and the impairments
appear to be specic to the right frontal (Cao et al., 2006) and parietal (Filipek et al., 1997) areas and to the associated connections
to subcortical structures, such as the limbic system (Stefanatos and
Wasserstein, 2001). Therefore, the disturbed microstructure in the
CC may also reect abnormalities of the left or right hemisphere
cells of origin. One EEG study using a simple reaction time laterality task found that, relative to healthy controls, ADHD patients
of the inattentive subtype showed slower right-to-left transfer,
whereas patients of the combined subtype exhibited faster leftto-right transfer, which demonstrated a lateralization dysfunction
in ADHD patients of different subtypes (Rolfe et al., 2007). Across
previous DTI studies in ADHD, altered FA was found in different
subdivisions of the CC of patients with ADHD (Chen et al., 2015;
Chuang et al., 2013; Onnink et al., 2015; van Ewijk et al., 2014). Our
meta-analysis suggested that the abnormal microstructure of the
splenium appears to be more robust than the other subdivisions
associated with this disorder. This nding is in line with previous meta-analyses of structural MRI studies (Putnam et al., 2010;
Seidman et al., 2005) that conclude that the volume reduction of
the posterior CC (including the splenium) was the most replicated
structural biomarker of children with ADHD.
We also found that the cluster in the CC splenium extended to
the right posterior cingulum, a limbic structure that carries major
efferent and afferent bers to the PCC and participates in attention
regulation (Langevin et al., 2014) and internally directed cognition
(Hahn et al., 2007). Previous diffusion studies that used methods
other than TBSS have also revealed that the cingulum shows altered
FA in patients with ADHD; however, the results are inconsistent
(Chen et al., 2015; Konrad et al., 2010; Makris et al., 2008). For
example, some studies that used VBA and tractography reported
lower FA in the cingulum of adults and youths with ADHD compared with healthy controls (Konrad et al., 2010; Makris et al.,
2008). Conversely, two other VBA studies found that children with
ADHD had higher FA scores than did healthy controls (Chen et al.,
2015; Peterson et al., 2011). Thus, the current ndings together
with previous evidence highlight the role that the limbic network
plays in ADHD and reveal that the reduced FA in the cingulum might
be more predominant across TBSS studies.
845
5. Limitations
Several limitations of the present study should be taken into
account. First, as is inherent in all coordinate-based methods,
our meta-analysis used the coordinates from the included studies
rather than the original t-statistic maps, which limits the accuracy of the results to a certain degree (Radua et al., 2012). Second,
two pairs of datasets used the same control samples (Cortese et al.,
2013; de Luis-Garca et al., 2015); however, because we focused on
the alterations in the patient groups, we considered this decision to
be appropriate. Third, because the effect sizes of unpublished studies are usually smaller than those of published studies (Lipsey and
Wilson, 1993), caution must be taken to not overestimate the overall effect sizes or SDM values. Given the numerous null results from
the studies that were included in the current meta-analysis, we
846
believe that this particular concern is minor. Finally, the main purpose of our subgroup analyses was to verify the ndings revealed
by the overall meta-analysis. Considering that the numbers of nonadult and male studies were relatively small (8 and 7 respectively),
the results of the subgroup analysis should be interpreted with
caution.
6. Conclusion
In conclusion, we qualitatively and quantitatively reviewed the
ndings of published TBSS studies on ADHD. Although these studies
differed in their sample characteristics and scanning procedures,
the use of TBSS enabled relatively high comparability across the
literature because its data processing and analyzing pipeline is relatively standardized. The increasing number of TBSS studies has
shown that a variety of WM tracts are affected in patients with
ADHD. The present meta-analysis of FA ndings found that the most
evident and consistent WM differences were located in the splenium of the CC extending to the right cingulum, the right SS and
left tapetum; furthermore, they involve the WM tracts that connect
the bilateral hemispheres, the occipital lobe-related neurocircuitry,
and the limbic system. In particular, altered microstructures in the
CC splenium and the right SS were robustly present in all sensitivity and subgroup analyses. These ndings suggest that, beyond the
classic fronto-striatal-cerebellar circuit, the left-right and posterior
brain WM pathways in the pathophysiology of ADHD deserve more
research attention.
Conicts of interest
All of the authors report no biomedical nancial interests or
potential conicts of interest.
Acknowledgements
This work was supported by the National Natural Science
Foundation (Grant Nos. 81171488, 81227002, and 81220108013),
the National Key Technologies R&D Program (Program No.
2012BAI01B03) and the Program for Changjiang Scholars and Innovative Research Team (PCSIRT, Grant No. IRT1272) in University of
China.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.neubiorev.2016.
07.022.
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