楊楠，任蕾，丁皓，肖茜，孫志華

低頻振幅結(jié)合功能連接對原發(fā)性甲亢患者感覺運(yùn)動(dòng)網(wǎng)絡(luò)的功能MRI研究

楊楠，任蕾，丁皓，肖茜，孫志華*

目的采用低頻振幅(amplitude of low frequency fluctuation，ALFF)與功能連接(functional connectivity，F(xiàn)C)相結(jié)合的方法，研究原發(fā)性甲狀腺功能亢進(jìn)患者靜息狀態(tài)下腦功能改變。材料與方法12名未經(jīng)治療的甲亢患者為病例組，12名自愿接受掃描的健康人(年齡、性別無顯著性差異)為對照組。采集所有被試靜息態(tài)fMRI數(shù)據(jù)，采用REST及DPARSF軟件分析原始數(shù)據(jù)，得出全腦ALFF，利用雙樣本t檢驗(yàn)的方法比較病例組和對照組 ALFF 的變化，并以兩組間ALFF值有顯著性差異的腦區(qū)為感興趣區(qū)(regions of interest，ROI)校正后行FC分析。結(jié)果與對照組相比，甲亢患者在雙側(cè)尾狀核及雙側(cè)丘腦ALFF值降低(P＜0.001)。以上腦區(qū)的ALFF值均未發(fā)現(xiàn)與T3、T4有顯著相關(guān)性(P＞0.05)。FC分析顯示，左側(cè)丘腦與雙側(cè)感覺運(yùn)動(dòng)區(qū)(包括中央前回、中央后回)FC增強(qiáng)(P＜0.001)；右側(cè)丘腦與右側(cè)中央前回及中央后回連接增強(qiáng)(P＜0.001)。結(jié)論甲亢患者雙側(cè)丘腦的局部活動(dòng)及其與大腦感覺運(yùn)動(dòng)網(wǎng)絡(luò)的FC模式存在異常，增強(qiáng)的FC可能與代謝損傷所導(dǎo)致運(yùn)動(dòng)機(jī)能受損而使甲狀腺功能異?；颊哂懈鼜?qiáng)的功能需求有關(guān)。

甲狀腺功能亢進(jìn)癥；磁共振成像；感覺運(yùn)動(dòng)網(wǎng)絡(luò)；低頻振幅；功能連接

甲狀腺激素異常是一類與神經(jīng)精神癥狀密切相關(guān)的內(nèi)分泌疾病[1-2]，對其發(fā)生神經(jīng)精神障礙病理生理機(jī)制的研究將有助于病情判斷及預(yù)后評估。在本研究中筆者采用低頻振幅(amplitude of low frequency fluctuation，ALFF)測量和功能連接(functional connectivity，F(xiàn)C)分析相結(jié)合的方法，探究甲狀腺功能亢進(jìn)患者引起局部神經(jīng)活動(dòng)的異常，及這些異常與功能網(wǎng)絡(luò)之間的關(guān)系。

1 材料與方法

1.1 受試者

搜集2014年6月至2016年8月在天津醫(yī)科大學(xué)總醫(yī)院核醫(yī)學(xué)科門診初診且未行治療的12例甲亢患者(男2例，女10例)臨床資料，年齡25～60 (41.75±10.5)歲。選擇同期選入的年齡及性別匹配的健康志愿者12例(男4例，女8例)為對照組，年齡35～50 (42.17±4.2)歲。納入標(biāo)準(zhǔn)：(1)男女均可，年齡大于等于18歲，右利手；(2)結(jié)合患者臨床癥狀及相關(guān)實(shí)驗(yàn)室檢查結(jié)果，符合原發(fā)性甲亢診斷標(biāo)準(zhǔn)的患者；(3)在獲得病人許可及家屬的知情同意后，接收入組。排除標(biāo)準(zhǔn)：(1)甲狀腺功能異常繼發(fā)于其他疾病的患者；(2)曾經(jīng)或當(dāng)前接受抗甲亢藥物治療的患者；(3)有其他的甲狀腺疾病的患者；(4)有其他內(nèi)分泌及自身免疫性疾病者；(5)精神狀況不穩(wěn)定或者曾經(jīng)有精神病病史的患者；(6)孕婦及處于哺乳期婦女；(7)患者如果有有嚴(yán)重的心臟、肝臟、腎臟功能障礙，也不允許入組；(8)有MRI檢查禁忌證者。所有被試均簽署了本實(shí)驗(yàn)知情同意書，且通過了天津醫(yī)科大學(xué)倫理委員會(huì)的批準(zhǔn)。

1.2 方法

詢問患者一般狀況并讓患者自愿填寫臨床資料表，包括性別、年齡、甲狀腺疾病病史、精神疾病家族史及臨床表現(xiàn)等。所有受試對象均在行頭顱磁共振掃描當(dāng)日，要求所有被試空腹，采取每個(gè)被試的肘靜脈血標(biāo)本，測定FT3、FT4及TSH (正常值范圍：FT3，3.5～6.5 pmol/L；FT4，11.5～23.5 pmol/L；TSH，0.3～5.0 μIU/mL)。

1.3 數(shù)據(jù)采集

采集功能MRI (fMRI)數(shù)據(jù)所使用的設(shè)備為由GE公司提供的3.0 T磁共振掃描儀(discovery MR750，General Electric，Milwaukee，WI，USA)，使用高分辨率8通道頭線圈。在實(shí)驗(yàn)開始前告知被試磁共振掃描所需的注意事項(xiàng)、禁忌以及大致掃描時(shí)間。掃描過程中被試仰臥于檢查床，用海綿填充頭部和線圈間的縫隙以最大限度地減少頭動(dòng)，為了減輕噪音給患者帶上大耳塞。對所有被試者先進(jìn)行常規(guī)軸面T1WI及T2WI，以排除顱內(nèi)器質(zhì)性病變，進(jìn)而進(jìn)行解剖及功能像的掃描。

3D高分辨率T1WI解剖像采用顱腦容積成像序列進(jìn)行矢狀面掃描。掃描參數(shù)如下：TR 8.2 ms，TE 3.2 ms；反轉(zhuǎn)時(shí)間(TI) 450 ms；反轉(zhuǎn)角(FA) 12°；FOV 256 mm×256 mm；矩陣 256×256；層厚1.0 mm，層數(shù)188，無間隔。

靜息態(tài)fMRI采用梯度回波單次激發(fā)回波平面成像(echo planar imaging，EPI)序列。掃描參數(shù)：TR 2000 ms，TE 45 ms；FOV 240 mm×240 mm；矩陣64×64；FA 90°；層厚4.0 mm，間隔0.5 mm；層數(shù)32層，采集180個(gè)時(shí)相。成像范圍覆蓋全腦。我們要求被試在掃描過程中閉上雙眼、保持平靜而均勻的呼吸、身體呈仰臥位保持不動(dòng)、盡量不要有任何思維活動(dòng)且保持清醒狀態(tài)。

1.4 fMRI數(shù)據(jù)處理

應(yīng)用DPARSF (Data Processing Assistant for Resting-State fMRI)軟件對每個(gè)被試的fMRI數(shù)據(jù)進(jìn)行預(yù)處理，具體的操作步驟：(1)將前10個(gè)時(shí)間點(diǎn)的數(shù)據(jù)去除，然后對剩余的170個(gè)時(shí)間點(diǎn)的數(shù)據(jù)進(jìn)行時(shí)間層校正及頭動(dòng)校正；(2)通過線性回歸的方式去除協(xié)變量；(3)圖像標(biāo)準(zhǔn)化，使用由SPM提供的標(biāo)準(zhǔn)EPI模板；(4)對標(biāo)準(zhǔn)化后的數(shù)據(jù)進(jìn)行空間平滑，使用8 mm×8 mm×8 mm的半高全寬(full width at half maximum，F(xiàn)WHM)高斯核。ALFF值計(jì)算采用基于Matlab的REST (www.restfmri.net)軟件，具體步驟如下：(1)首先進(jìn)行時(shí)間序列到頻率范圍的轉(zhuǎn)換，利用的是傅里葉變換方法，然后獲得每個(gè)頻率的功率譜并計(jì)算出其平方根，最后求所有平方根的平均值，這就是所要的ALLF值；(2)對ALLF值進(jìn)行標(biāo)準(zhǔn)化以降低個(gè)體差異對結(jié)果的影響，用每個(gè)體素的ALFF值除以全腦ALFF值的平均值就得到了ALFF的標(biāo)準(zhǔn)化值(mALFF)；(3)所得數(shù)據(jù)重釆樣，體素大小為2 mm×2 mm×2 mm。最后獲得所有被試者在靜息狀態(tài)下ALFF激活圖，然后采用雙樣本t檢驗(yàn)的統(tǒng)計(jì)方法比較兩組被試ALFF值，檢驗(yàn)標(biāo)準(zhǔn)P＜0. 001(AlphaSim校正)。

1.5 統(tǒng)計(jì)分析

采用REST (www.restfmri.net)軟件自帶的統(tǒng)計(jì)分析軟件對病例組與對照組ALFF數(shù)據(jù)進(jìn)行雙樣本t檢驗(yàn)(P＜0.001，AlphaSim校正)。然后選取上述兩組間 ALFF 值存在顯著性差異的腦區(qū)為感興趣區(qū)(region of interest，ROI)，做全腦的基于體素的FC，并分析兩組間FC的差異。最后使用Pearson相關(guān)分析方法檢驗(yàn)ALFF值與血清FT3、FT4是否存在相關(guān)性，統(tǒng)計(jì)結(jié)果必須滿足P值小于0.05才能說明相關(guān)。

2 結(jié)果

2.1 靜息態(tài)ALFF

經(jīng)rfMRI數(shù)據(jù)ALFF法分析，與正常對照組相比，甲亢組在雙側(cè)尾狀核及雙側(cè)丘腦ALFF值較由健康志愿者組成的對照組明顯降低(P＜0.001，AlphaSim校正)(表1，圖1)；三個(gè)腦異常功能區(qū)ALFF值與T3、T4間相關(guān)性無統(tǒng)計(jì)學(xué)差異(P＞0.05)。

2.2 FC

分別以左側(cè)尾狀核，左側(cè)丘腦及右側(cè)丘腦為ROI做全腦FC，并比較兩組間每個(gè)ROI與全腦FC的差異，結(jié)果顯示左側(cè)丘腦與雙側(cè)感覺運(yùn)動(dòng)網(wǎng)絡(luò)(包括中央前回、中央后回)，左側(cè)額上回、左側(cè)顳上回及左側(cè)顳下回FC明顯增強(qiáng)(P＜0.001，AlphaSim校正)(表2，圖2A)。右側(cè)丘腦與右側(cè)中央前回及中央后回FC明顯增強(qiáng)(P＜0.001，AlphaSim校正)(表2，圖2B)。左側(cè)尾狀核與全腦FC在兩組被試之間未發(fā)現(xiàn)明顯差異。

3 討論

甲狀腺功能亢進(jìn)癥(甲亢) 是一種臨床上經(jīng)常遇到的與精神神經(jīng)癥狀相關(guān)的內(nèi)分泌疾病，甲狀腺激素對腦的發(fā)育有深刻的影響[3-6]。所以甲狀腺功能異?；颊叱０橛懈杏X運(yùn)動(dòng)功能障礙、視覺功能障礙以及情緒、認(rèn)知功能障礙等神經(jīng)精神癥狀的表現(xiàn)[7]。感覺運(yùn)動(dòng)功能障礙方面，甲亢患者常出現(xiàn)肌肉持續(xù)性震顫及乏力[8]。

隨著MRI技術(shù)的創(chuàng)新應(yīng)用及不斷發(fā)展，fMRI已被大家普遍認(rèn)為是探究甲狀腺激素異?；颊叩囊环N重要方法，它能發(fā)現(xiàn)甲狀腺激素異?；颊邼撛诘哪X功能及結(jié)構(gòu)改變[9-11]。ALFF 是低頻范圍內(nèi)功率譜的平方根，它從能量代謝角度測量每個(gè)體素的波動(dòng)強(qiáng)度，也就是說ALFF值能直接反映大腦各區(qū)域神經(jīng)元自發(fā)活動(dòng)[12]。而FC討論的則是各個(gè)腦區(qū)之間代謝活動(dòng)在時(shí)間序列上的相關(guān)性。FC可以從整體上顯示各腦區(qū)間的FC，但不能反映具體哪個(gè)腦區(qū)的自發(fā)活動(dòng)有異常改變。本實(shí)驗(yàn)結(jié)合ALFF及FC兩種分析方法，對甲亢患者的局部神經(jīng)活動(dòng)及整體FC進(jìn)行評價(jià)[13-14]。

在本項(xiàng)研究中我們發(fā)現(xiàn)甲亢組雙側(cè)尾狀核ALLF值較正常對照組ALFF值明顯降低，說明雙側(cè)尾狀核自發(fā)性腦活動(dòng)減弱。尾狀核作為紋狀體的重要組成部分，參與紋狀體-黑質(zhì)環(huán)路的構(gòu)成[15]，來自黑質(zhì)致密部的多巴胺輸入刺激紋狀體內(nèi)的多巴胺受體，而甲狀腺激素可以加速腦多巴胺的代謝，修飾多巴胺受體以影響其敏感性。筆者猜測這種作用機(jī)制可能在一定程度上影響了雙側(cè)尾狀核的功能，從而出現(xiàn)ALFF值減低的現(xiàn)象。

表1 病例組ALFF異常的腦區(qū)與對照組比較Tab. 1 Regions showing differences in ALFF between groups

表2 病例組FC異常的腦區(qū)與對照組比較Tab. 2 Regions showing differences in FC between groups

圖1 與對照組比較病例組ALFF值異常的區(qū)域(P＜0.001, AlphaSim校正)。A：冠狀面；B：矢狀面；C：橫軸面圖2 與對照組比較病例組FC增強(qiáng)的區(qū)域(P＜0.001，AlphaSim校正)。A：以左側(cè)丘腦為ROI，F(xiàn)C增強(qiáng)的區(qū)域(P＜0.001，AlphaSim校正)。B：以右側(cè)丘腦為ROI，F(xiàn)C增強(qiáng)的區(qū)域(P＜0.001，AlphaSim校正)Fig. 1 Regions showing differences in ALFF between groups (P＜0.001, AlphaSim corrected). A: Coronal image. B: Sagittal image. C: Transverse image.Fig. 2 Regions showing differences in FC between groups (P＜0.001, AlphaSim corrected). A: Regions showing differences in FC of the left-thalamus-ROI between groups (P＜0.001, AlphaSim corrected). B: Regions showing differences in FC of the right-thalamus-ROI between groups (P＜0.001, AlphaSim corrected).

人腦中許多復(fù)雜的活動(dòng)都依賴于大腦皮質(zhì)及皮質(zhì)下廣泛區(qū)域之間的相互聯(lián)系，而丘腦與大腦中諸多腦區(qū)均存在著明顯的FC，可以說丘腦是大腦中具有重要功能的信息處理及交換中心[16]。Alexander等[17]提出了基底核-丘腦-皮層環(huán)路的概念，丘腦經(jīng)丘腦輻射與大腦皮層連接。以往研究表明甲亢患者常具有感覺運(yùn)動(dòng)、視覺及情緒認(rèn)知障礙等神經(jīng)精神癥狀。而這些功能的完成均需依賴丘腦這一信息中繼站。1999年Khushu等[18]發(fā)現(xiàn)，在一項(xiàng)執(zhí)行手指敲擊任務(wù)的fMRI試驗(yàn)中，正常對照組在對側(cè)初級運(yùn)動(dòng)皮層、輔助運(yùn)動(dòng)區(qū)及軀體感覺區(qū)等區(qū)域有明顯激活，而甲亢患者較正常對照組相比非但這些區(qū)域的激活體積增大，而且出現(xiàn)了雙側(cè)激活。在本實(shí)驗(yàn)中我們發(fā)現(xiàn)甲亢患者雙側(cè)丘腦ALFF值減低，且左側(cè)丘腦與雙側(cè)大腦感覺運(yùn)動(dòng)區(qū)(包括中央前回、中央后回)，右側(cè)丘腦與右側(cè)大腦感覺運(yùn)動(dòng)區(qū)(包括右側(cè)中央前回及中央后回)FC增強(qiáng)。筆者認(rèn)為這可能與代謝損傷所導(dǎo)致運(yùn)動(dòng)機(jī)能受損而使甲狀腺功能異常患者有更強(qiáng)的功能需求有關(guān)[19]。

以往對于甲狀腺功能異常患者的fMRI研究，多數(shù)實(shí)驗(yàn)結(jié)果都集中闡明其情緒認(rèn)知障礙與腦功能及結(jié)構(gòu)之間的關(guān)系[20-25]，而鮮有研究報(bào)導(dǎo)甲亢患者感覺運(yùn)動(dòng)網(wǎng)絡(luò)的改變及其與臨床上感覺運(yùn)動(dòng)障礙之間的聯(lián)系。本研究中利用ALFF與FC相結(jié)合的方式發(fā)現(xiàn)甲亢患者丘腦與感覺運(yùn)動(dòng)皮層之間FC增強(qiáng)，提示甲亢患者運(yùn)動(dòng)功能障礙與腦功能改變之間的相關(guān)性，今后可增加被試量及臨床運(yùn)動(dòng)障礙方面研究以進(jìn)一步分析甲亢患者感覺運(yùn)動(dòng)功能損傷機(jī)制。

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A fMRI study on the amplitude of low-frequency fl uctuation and functional connectivity in resting-state of sensorimotor network of primary hyperthyroidism individuals

YANG Nan, REN Lei, DING Hao, XIAO Qian, SUN Zhi-hua*
Department of Radiology, Tianjin Medical University General Hospital, Tianjin 300052, China
*Correspondence to: Sun ZH, E-mail: dr_zhihuasun@sina.com

Objective:To investigate the changes of ALFF (amplitude of lowfrequency fluctuation) and FC (functional connectivity) in hyperthyroid patients with RS-fMRI (resting-state functional magnetic resonance imaging), and the relationships of the characteristics with emotional disorders, spontaneous brain resting activities, biochemical and biological characteristics.Materials and Methods:Twelve patients diagnosed with primary hyperthyroidism were collected in this study. Another 12 age-and-sex-matched healthy individuals served as control. Gathering fMRI scaned of all the subjects at their resting -state, using REST and DPARSF software to obtain each amplitude of low-frequency fluctuation (ALFF), then we used two samplet-test to discover the brain areas with signif i cant differentiation of ALFF values. The brain areas were def i ned as regions of interest (ROI). ROI based functional connectivities (FC) were analyzed to explore some possible abnormalities.Results:Compared with controls, the ALFF of hyperthyroidism individuals was reduced in the bilateral caudate, and bilateral thalamus (P＜0.001). In these brain regions, we find no correlation between ALFF and T3, T4 (P＞0.05). In contrast with controls, hyperthyroid patients showed stronger FC between the left thalamus and both the bilateral precentral gyrus and bilateral postcentral gyrus (P＜0.001), as well as between the right thalamus and both the right precentral gyrus and right postcentral gyrus (P＜0.001).Conclusions:The present study shows that, functional demands between bilateral thalamus and sensorimotor network are higher in patientscompared to controls. It is likely attributed to motor function deficit associated with metabolic impairment in these patients.

Hyperthyroidism; Magnetic resonance imaging; Sensorimotor network; Amplitude of low frequency fluctuation; Functional connectivity

國家自然科學(xué)基金青年基金(編號：81201152)

天津醫(yī)科大學(xué)總醫(yī)院醫(yī)學(xué)影像科，天津 300052

孫志華，E-mail：dr_zhihuasun@sina. com

2016-11-07

接受日期：2017-01-06

R445.2；R581

A

10.12015/issn.1674-8034.2017.03.008

楊楠, 任蕾, 丁皓, 等. 低頻振幅結(jié)合功能連接對原發(fā)性甲亢患者感覺運(yùn)動(dòng)網(wǎng)絡(luò)的功能MRI研究. 磁共振成像, 2017, 8(3): 204-108.

Received 7 Nov 2016, Accepted 6 Jan 2017

ACKNOWLEDGMENTSThis work was supported by the National Natural Science Foundation of China (No. 81201152).