The Journal of Pain, Vol 14, No 12 (December), 2013: pp 1703-1708 Available online at www.jpain.org and www.sciencedirect.com

Migraine-Related Gray Matter and White Matter Changes at a 1-Year Follow-Up Evaluation Jixin Liu,* Lei Lan,y Guoying Li,* Xuemei Yan,* Jiaofen Nan,* Shiwei Xiong,* Qing Yin,* Karen M. von Deneen,* Qiyong Gong,z Fanrong Liang,y Wei Qin,* and Jie Tian* *School of Life Sciences and Technology, Xidian University, Xi’an, China. y The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu, China. z Department of Radiology, The Center for Medical Imaging, Huaxi MR Research Center (HMRRC), West China Hospital of Sichuan University, Chengdu, Sichuan, China.

Abstract: To assess the longitudinal gray matter (GM) and white matter (WM) changes between repeated observations 1 year apart in a group of the early clinical stage of migraine patients without aura, and to explore the relationship of such structural changes with headache activity, we studied patients newly diagnosed with episodic migraine lasting 8 to 14 weeks. Optimized voxel-based morphometry and tract-based spatial statistical analyses were used to evaluate changes in GM and WM by using 3-dimensional T1-weighted and diffusion-tensor imaging, respectively. At the 1-year follow-up examination, GM reduction was observed in the dorsolateral and medial part of the superior frontal gyrus, orbitofrontal cortex, hippocampus, precuneus, and primary and secondary somatosensory cortices. No significant differences were found in the fractional anisotropy and longitudinal, radial, and mean diffusivity of WM in migraine patients without aura within a year. Negative results were found for the association between changes in headache activity parameters and GM. Our results indicated that the GM and WM changed in different pathophysiological conditions of migraine patients without aura. The WM probably evolves slowly in the course of migraine chronicity. Perspective: Our study found early involvement of GM reduction of sensory-discriminative brain regions in the pathologic process of migraine, but the WM did not exhibit significant changes in the same time interval. GM reduction in sensory-discriminative brain regions may characterize the pathophysiological features of migraine patients without aura in its early stage. Crown Copyright ª 2013 Published by Elsevier Inc. on behalf of the American Pain Society Key words: MRI, gray matter, white matter, 1-year follow-up examination, migraine.

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igraine, as the most common neurologic disease, causes a significant individual and societal burden because of recurrent moderate to severe pain, resulting in disability and aggravation by physical activity.36 Although structural neuroimaging has led to advances in the description of migraine Received May 31, 2013; Revised July 30, 2013; Accepted August 24, 2013. This paper is supported by the Project for the National Key Basic Research and Development Program (973) under Grant nos. 2012CB518501 and 2011CB707700, the National Natural Science Foundation of China under Grant nos. 81227901, 81271644, 30930112, 81000640, 81000641, 81101036, 81101108, 81030027, and 31200837 and the Fundamental Research Funds for the Central Universities. The authors declare no conflicts of interest. Authors Jixin Liu and Lei Lan contributed equally to this work. Address reprint requests to Wei Qin, PhD, School of Life Sciences and Technology, Xidian University, Xi’an 710071, Peoples R. China. E-mail: [email protected] 1526-5900/$36.00 Crown Copyright ª 2013 Published by Elsevier Inc. on behalf of the American Pain Society http://dx.doi.org/10.1016/j.jpain.2013.08.013

mechanisms and found changes in brain morphology,26,36 the identified alterations act as a diathesis for migraine or are ascribable to the transmission of headache, which is largely unclear. Moreover, whether or not the changes could serve as an indicator in migraine transformation has not yet been fully studied. Magnetic resonance imaging (MRI) techniques attempt to find reliable neurologic markers in migraine, including the evaluation of gray matter (GM) and white matter (WM). Several independent studies have pointed out that migraine has a decreased intensity in GM in pain-transmitting areas.20,32,34,35,41 With the help of diffusion tensor imaging techniques, our group previously found significantly lower fractional anisotropy (FA), mean diffusivity (MD), and axial diffusivity (AD) in multiple brain regions in patients with migraine.42 In addition, some of the brain structural changes were more or less correlated with disease duration and headache frequency. Researchers discussed 1703

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these findings as atrophy and axonal loss in migraineurs.20,32,42 Moreover, when investigators of recent cross-sectional studies compared the GM and WM density between patients with a high attack frequency and longer duration of migraine and those with a lower frequency and shorter headache attacks, the significant between-group differences were found in the prefrontal cortex, limbic system–related brain regions, basal ganglia, and parietal lobes.35,36 These studies indicated that patients with migraine have selective alterations in GM and WM involved in central pain processing, which may reflect cumulative brain insults from infrequent to frequent cortical overstimulation associated with disease duration and headache frequency.22-24,26,36,42 However, the exact process underlying these structure changes has not been fully understood, and changes that precede, and therefore predict, the transition when the clinical syndromes fall into a relatively more severe stage is still unknown. In our study, we used structural imaging technology to assess the longitudinal changes in GM and WM in a cohort study of the early clinical stage in migraine patients without aura (MWoA) who were observed for 1 year. Voxel-based morphometry (VBM) and tract-based spatial statistical (TBSS) analyses were used to evaluate the changes in GM and WM.

Methods All research procedures were approved by the West China Hospital Subcommittee on Human Studies and were conducted in accordance with the Declaration of Helsinki. Written informed consent was obtained from each participant.

Participants All of the patients fulfilled the International Classification of Headache Disorders, 2nd Edition (ICHD-II) criteria. Inclusion criteria for the migraine patients group were according to ICHD-II MWoA17: 1) featuring at least 2 of the following characteristics: unilateral location, pulsating quality, moderate-tosevere pain intensity, and aggravation by causing avoidance of routine physical activity; 2) headache attacks last 4 to 72 hours (untreated or unsuccessfully treated); 3) there is nausea and/or vomiting, photophobia, and phonophobia during headache; and 4) headache is disabling. Exclusion criteria were 1) macroscopic brain T2-visible lesions on MRI scans; 2) existence of a neurologic disease; 3) pregnancy; 4) alcohol, nicotine, or drug abuse; and 5) claustrophobia. We studied newly diagnosed patients with episodic migraine lasting 8 to 14 weeks. Thirty-six patients were consecutively enrolled in the current study. Patients participated in 2 image scanning sessions 1 year apart (mean duration = 371 days; range = 351–386 days) by using the same MRI and acquisition protocol. Detailed information about the patients’ headache diary and drug intake was obtained before each imaging scan. Some migraine patients who completed the study were removed from the analysis because of missing data.

Longitudinal Brain Structural Changes in Migraine The remaining 21 patients (age = 22.6 6 2.0 years; height = 161.75 6 3.6 cm; weight = 53.2 6 5.7 kg) were included in the study.

Headache Activity and Mood Rating Patients were required to keep a headache diary to record their headache activity in the past 4 weeks before the MRI scans, including the migraine attack frequency (number of times), migraine attack duration (hours), and average pain intensity of the headache (0–10 scale, with 10 being the most intense pain imaginable). The Zung Self-Rating Anxiety Scale and Zung Self-Rating Depression Scale were used to quantify the anxiety/depression-related symptoms of the patients. Both of the scales consist of 20 items, and each item is scored from 1 to 4. Based on the Chinese norm,10 an index score of Zung Self-Rating Anxiety Scale (calculated by multiplying the raw score by 1.25) being less than 50 or an index score of the Zung Self-Rating Depression Scale (calculated by multiplying the raw score by 1.25) being less than 53 falls into the normal range.

Medication Subjects were allowed to have pirprofen when their headache was difficult to endure. Six patients also used opiates (Percocet; Endo Pharmaceuticals, Shen Yang, Lio Ning, China). Other patients received no treatment. Detailed information about patients’ drug intake for the prevention of migraine was obtained. The Medication Quantification Scale was used to quantify the consumption of the drug in the past 4 weeks before each visit, and the dosage and duration of the drug used could be represented by a scalar value.

Imaging Acquisition This experiment was carried out in a 3.0-Tesla Signa GE scanner (GE Healthcare, Milwaukee, WI) with an 8-channel phase array head coil at the Huaxi MR Research Center in Sichuan, China. For each subject, a high-resolution structural image was acquired by using a 3-dimensional MRI sequence with a voxel size of 1 mm  1 mm  1 mm using an axial fast spoiled gradient recalled sequence with the following parameters: repetition time = 1,900 ms; echo time = 2.26 ms; data matrix = 256  256; field of view = 256 mm  256 mm. The diffusion tensor images were obtained with a single-shot echo-planar imaging sequence. The diffusion sensitizing gradients were applied along 30 noncollinear directions (b = 1,000 s/mm2) with an acquisition without diffusion weighting (b = 0 s/mm2). The imaging parameters were 45 continuous axial slices with a slice thickness of 3 mm and no gap, field of view = 240 mm  240 mm; repetition time = 6,800 ms; echo time = 93 ms; data matrix = 128  128. Diffusion tensor images were acquired with 2 averages.

Data Analysis Data preprocessing was carried out using the Oxford Centre for Functional Magnetic Resonance Imaging of

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the Brain (FMRIB)’s Diffusion Toolbox (FDT) 2.0 and parts of the FMRIB Software Library (FSL) 4.1.9 (Oxford Centre for Functional Magnetic Resonance Imaging of the Brain Software Library, www.fmrib.ox.ac.uk/fsl/).

our study (5,000 random permutations). For multiple comparison corrections, the threshold-free cluster enhancement with the family-wise error correction was employed.28

VBM Analysis

Results

First, all T1 images were brain extracted using the brain extracting tool (BET).39 Second, tissue-type segmentation was carried out using the FMRIB’s automated segmentation tool (FAST) v4.1.43 The resulting GM partial volume images were then aligned to Montreal Neurological Institute 152 standard space using the FMRIB’s linear image registration tool (FLIRT),18,19 followed by nonlinear registration using FMRIB’s nonlinear image registration tool as optional (FNIRT).1,2 Third, the resulting images were averaged to create a study-specific template to which the native GM images were nonlinearly re-registered. The optimized protocol introduced a modulation for the contraction/enlargement caused by the nonlinear component of the transformation: each value of the voxel in the registered GM image was divided by the Jacobian of the warp field. Fourth, to choose the best smoothing kernel, all modulated, normalized GM volume images were smoothed with isotropic Gaussian kernels increasing in size (s = 2.5, 3, 3.5, and 4 mm corresponding to full widths at half-maximum of 6, 7, 8, and 9.2 mm, respectively). Finally, regional changes in GM were assessed using permutation-based nonparametric testing with 5,000 random permutations. Correction for multiple comparisons was carried out using a cluster-based thresholding method, with an initial cluster forming a threshold at t = 2.0.

TBSS Analysis First, the BET was used for brain extraction.39 Second, the eddy current distortion and head motion of raw diffusion data were corrected using FDT. Third, FA, MD, and eigenvalue maps were calculated by fitting a tensor model at each voxel of the diffusion data using FDT. An AD image was the first eigenvalue (L1) map, and radial diffusivity (RD) images were calculated via the mean of the second and third eigenvalue maps. Fourth, TBSS analyses were performed.28 All FA images were nonlinearly registered to an FMRIB58-FA standardspace template (FMRIB Centre University of Oxford, Department of Clinical Neurology, John Radcliffe Hospital Headington, Oxford, United Kingdom; http:// www.fmrib.ox.ac.uk/fsl/data/FMRIB58_FA.html) and aligned to the Montreal Neurological Institute space. The mean image of all aligned FA images was created and thinned (non-maximum-suppression perpendicular to the local tract structure) to create a skeletonized mean FA image, which was thresholded at the FA value of .2.28 Then, the aligned FA image was projected onto this skeleton. The MD, RD, and AD images were also aligned into Montreal Neurological Institute space and projected onto the mean FA skeleton. Finally, the permutation-based nonparametric inferences were used to detect the between-group differences in

Clinical Variables At the 1-year follow-up, the headache attack frequency in MWoA was statistically higher than the prior level (mean 6 standard deviation = 4.4 6 2.3; 9.5 6 4.7 times, P = .001, Fig 1). There were no significant differences in patients’ attack duration (P = .2) and average pain intensity (P = .5) (Table 1). According to the Zung Self-Rating Anxiety Scale and the Zung Self-Rating Depression Scale assessment, patients showed a similar mood characteristic between the 2 visits (P > .05), and no patients exhibited mild or major depression and anxiety (Table 1).

Changes in Brain GM and WM The VBM longitudinal analysis found a significant GM decrease in several brain regions at the 1-year follow-up examination (P < .05, family-wise error corrected; Fig 2), including the dorsolateral and medial part of the superior frontal gyrus, orbitofrontal cortex, hippocampus, precuneus, inferior parietal gyrus, superior parietal gyrus, postcentral gyrus, paracentral lobule, and supramarginal gyrus. These differences persisted after controlling for the medication effect. To further characterize the structural alterations found in MWoA, we performed a correlation analysis between changes in clinical variables and local GM. Negative results were found for the association between changes in headache activity parameters and the observed GM. The analysis of FA, MD, AD, and RD revealed no threshold-free cluster enhancement–corrected suprathreshold voxels. No significant difference was found even when the threshold was set at .05 uncorrected. These results persisted after controlling for the medication effect.

Figure 1. MWoA had a significantly increased migraine attack frequency (*P = .001).

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Clinical Characteristics of Patients at Baseline and 1-Year Follow-Up

Table 1.

PATIENTS WITH MIGRAINE (N = 21) INFORMATION

BASELINE

FOLLOW-UP

P VALUE

Attack duration (hours) Attack frequency (times) Average pain intensity Anxiety (SAS) Depression (SDS)

8.2 6 5.9 4.4 6 2.3 5.6 6 .8 41.4 6 6.0 42.7 6 8.1

6.7 6 3.3 9.5 6 4.7 5.3 6 1.4 40.5 6 6.5 39.3 6 7.1

.2 .001 .5 .2 .1

Abbreviations: SAS, Zung Self-Rating Anxiety Scale; SDS, Zung Self-Rating Depression Scale.

Discussion Several studies pointed out that the properties of the clinical conditions of chronic pain were influencing the brain’s GM and WM.4,5,15,21 Conversely, the brain’s structure could dynamically reflect the pain state.16,33,37 Improved understanding of the neural reorganization and relationship between GM and WM damage that mediates pain chronification may have vast clinical implications for the treatment of migraine.33 Although lacking patients in the earliest stages of migraine, the question arises whether the GM and WM change in different pathophysiological conditions in the course of migraine chronification and whose temporal evolution is present first in the transmission of headache. Hence, by using the VBM and TBSS analysis, we aimed to investigate longitudinal changes in GM and WM of patients with the early phase of migraine in the present study. The main finding was that at 1-year follow up, MWoA had a decreased GM in the dorsolateral part of the prefrontal cortex, orbitofrontal cortex, and primary and secondary somatosensory cortices. As already described in other literature, pain is a complex and subjective experience that is shaped by evaluation and judgments about afferent sensory information.9,28 Current conceptual models of pain processing restrict the sensory-discriminative property to the lateral pain system,28 which consists of the primary and secondary somatosensory cortices 11,30 that encode the location, intensity, and quality of sensations of pain and connect to the posterior parietal cortex that conveys widespread nociceptive information to widespread cortical brain regions9 and may provide modulatory influences on the large prefrontal cortex in pain modulation.4 The significant GM loss in these brain regions in our results suggested that the abnormal morphological changes in MWoA may first appear in the pain-sensory areas in the course of the migraine. That is, if migraine was present in the disease onset, the sensory-discriminative dimension may dominate the pain experience and processing and the affectivemotivational and cognitive-evaluative dimensions may be less significant. Additionally, progressive regions of reduced GM density related to processing of the perception and unpleasant-affective dimension of pain

Figure 2. Decreased GM at the 1-year follow-up in MWoA (P < .05, family-wise error corrected). GM reduction was found in the dorsolateral and medial part of the superior frontal gyrus, orbitofrontal cortex, hippocampus, precuneus, inferior parietal gyrus, superior parietal gyrus, postcentral gyrus, paracentral lobule, and supramarginal gyrus. have been reported in patients with episodic migraine and chronic long-term headache in cross-sectional studies.35,41 We hypothesized that the transition from the initial stage of migraine to chronic pain may involve a time-dependent neural reorganization, and such temporal development may involve the interaction between light to heavy/infrequent to frequent headaches and headache experience–related reorganization that together shift brain functional subnetworks to distinct states in specific clinical conditions.3 To our knowledge, our study represented the first dynamic alteration of brain morphology evolution within the first year of the initial stage of migraine. Compared with the baseline, MWoA had a reduction in GM in the precuneus, medial part of the prefrontal cortex, and hippocampus. These regions were commonly observed in the default mode networks (DMNs), which were particularly sensitive to cognitive states in self-referential tasks.38 Several studies found that DMN-related functional connections were altered across the pain population, including diabetic neuropathy, fibromyalgia, and chronic back pain.6,8,13,27 Recently, Loggia et al25 pointed out that the DMN could encode the intensity of clinical pain both at baseline and in response to maneuvers aimed at exacerbating clinical pain levels; moreover, they also found that the DMN predicted postmaneuver lingering pain in chronic low back pain patients. Because the function of DMN activity is critical in human consciousness,7 the decreased GM we found during the first year after the clinical early phase of migraine may reflect the presence of ongoing pain, which could be viewed as the extent to which episodic headache interferes with information processing and intrinsic variations in brain activity.13 Regional GM changes may reflect the local extracellular alteration in water or contribute to the changes in the concentration of the channels of proteins within neurons and glia. Hence, the microstructural properties connected to the regional neurons involved need to be considered; if the GM reduction was caused by neuronal death, the corresponding WM density or

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connectivity should also be modified, reflecting such changes.4 However, in our results no significant WM alteration was found. As compared with healthy controls, changes in WM microstructure have been reported in migraine by a number of studies.12,31,40 A 3-year longitudinal study revealed that the WM lesion number progressed over time in migraine with aura. These results indicated that WM alterations may be implicated in the pathophysiology of migraine.36 In contrast, the longitudinal analysis presented here did not find any changes in the FA, MD, AD, and RD of the WM in MWoA within a year. One inference from our results was that GM and WM changed in different pathophysiological conditions in MWoA. Although chronic migraine could lead to abnormal changes in the GM and WM for the long-term and highfrequency nociceptive input, we inferred that the pathophysiological features of MWoA in the early stage may be characterized by GM reduction. The WM probably evolves slowly in the course of migraine chronification and has a less influential role than GM for migraine progression. Over time, when the localization of sensory-discriminative dimension of pain became

vaguer and the cognitive and affective dimensions became more prominent for the severe clinical migraine outcome, patients could fall into the chronic pain state, with significant alteration in WM.14,29 Nevertheless, we did not find any association between changes in headache activity and intensity of the GM in our study. Inconsistent results for the association between headache activity and brain structural changes have been reported in migraine studies,29,35,40,41 which remain a matter of debate. So far, there has been little imaging data at multiple time points regarding the dynamic pathomechanism of brain structural changes during the first year after the early clinical stage of migraine. Our study found the early involvement of GM reduction of sensory-discriminative brain regions in the pathologic process of migraine, but the WM did not exhibit significant changes in the same time interval. These findings indicated that the alteration in GM and WM may take place at different pathophysiological points in migraine. If our results are replicated in a large sample, it may help us better understand the progression of migraine and implicate its treatment.

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Migraine-related gray matter and white matter changes at a 1-year follow-up evaluation.

To assess the longitudinal gray matter (GM) and white matter (WM) changes between repeated observations 1 year apart in a group of the early clinical ...
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