胡磊，查云飛，林苑，邢棟，龔?fù)蹩塑?，閆力永，王嬌

IDEAL-IQ定量評(píng)價(jià)兔糖尿病模型椎體骨髓脂肪含量的可行性研究

胡磊，查云飛*，林苑，邢棟，龔?fù)蹩塑?，閆力永，王嬌

目的 探索定量非對(duì)稱回波的最小二乘估算法迭代水脂分離序列(iterative decomposition of water and fat with echo asymmetry and least-squares estimation quantitation sequence，IDEAL-IQ)定量評(píng)估兔糖尿病模型椎體骨髓脂肪含量的可行性。材料與方法 12只3月齡新西蘭雄性大白兔隨機(jī)分為糖尿病組(n=6)和對(duì)照組(n=6)。用四氧嘧啶對(duì)糖尿病組造模，在造模成功后各時(shí)間點(diǎn)(0、4、8、12、16周)，對(duì)糖尿病組及對(duì)照組行腰椎矢狀位T1WI、T2WI、IDEAL-IQ檢查。在IDEAL-IQ脂肪分?jǐn)?shù)圖像測量興趣區(qū)內(nèi)脂肪含量比值；在16周處死糖尿病組和對(duì)照組的大白兔，取腰3～7椎體做HE染色脂肪細(xì)胞計(jì)數(shù)；對(duì)實(shí)驗(yàn)組和對(duì)照組兔各時(shí)間點(diǎn)的脂肪含量比值采用重復(fù)測量的方差分析；對(duì)16周實(shí)驗(yàn)組和對(duì)照組IDEAL-IQ測量腰椎體脂肪比參數(shù)與HE切片鏡下脂肪細(xì)胞計(jì)數(shù)行Pearson相關(guān)分析。結(jié)果 16周實(shí)驗(yàn)組兔腰椎常規(guī)矢狀位T1WI和T2WI顯示諸腰椎椎體信號(hào)輕度增高。常規(guī)HE染色顯示，16周糖尿病組兔椎體終板下骨髓腔脂肪含量較對(duì)照組明顯增多，骨髓細(xì)胞明顯減少。糖尿病組各時(shí)間節(jié)點(diǎn)椎體骨髓的脂肪含量比值差異存在統(tǒng)計(jì)學(xué)意義(F=50.387，P＜0.01)，對(duì)照組各時(shí)間點(diǎn)脂肪含量比值差異不存在統(tǒng)計(jì)學(xué)意義(F=1.477，P＞0.05)；16周實(shí)驗(yàn)組與對(duì)照組的椎體骨髓脂肪含量比值(FF%)差異有統(tǒng)計(jì)學(xué)意義(t=-10.726，P＜0.01)；IDEAL-IQ測量椎體脂肪含量比與脂肪細(xì)胞計(jì)數(shù)高度正相關(guān)關(guān)系(r=0.925，P＜0.05)。結(jié)論 IDEALIQ定量評(píng)估兔糖尿病模型椎體骨髓脂肪含量是可行的。

糖尿病，實(shí)驗(yàn)性；骨髓；脂肪定量；磁共振成像；實(shí)驗(yàn)動(dòng)物科學(xué)；兔

糖尿病脂質(zhì)代謝紊亂導(dǎo)致的高膽固醇、高甘油三酯血癥以及多不飽和脂肪酸與骨髓細(xì)胞減少、微血管病變和骨質(zhì)疏松等密切相關(guān)[1-3]，糖尿病患者容易罹患骨質(zhì)疏松、病理性骨折等疾病[4-5]。骨髓脂肪已經(jīng)成為糖尿病骨髓病變的生物標(biāo)志物，活體定量評(píng)價(jià)骨髓脂肪含量對(duì)于揭示糖尿病骨代謝及骨髓微血管病變病理生理機(jī)制具有重要的意義。

磁共振骨髓脂肪定量技術(shù)在監(jiān)測骨髓脂肪變化和判斷骨髓功能狀態(tài)方面具有獨(dú)特優(yōu)勢。氫質(zhì)子磁共振波譜分析的缺點(diǎn)在于掃描條件要求高，時(shí)間長，尤其在骨骼系統(tǒng)不甚穩(wěn)定，且后處理過程十分繁瑣，限制該技術(shù)的發(fā)展應(yīng)用[6]。定量非對(duì)稱回波的最小二乘估算法迭代水脂分離序列(iterative decomposition of water and fat with echo asymmetry and least-squares estimation quantitation sequence，IDEAL-IQ)技術(shù)作為改進(jìn)的DIXON成像，經(jīng)過T2*衰減的修正和脂肪的多譜峰分布，在IDEAL技術(shù)的基礎(chǔ)上把定性的水脂分離提高到定量的脂肪比例測量，該技術(shù)在活體骨髓脂肪含量的定量研究中顯示了巨大優(yōu)勢[7-8]。

目前，尚未見IDEAL-IQ技術(shù)評(píng)價(jià)糖尿病骨髓脂肪含量的相關(guān)研究，本研究探討IDEAL-IQ定量評(píng)價(jià)兔糖尿病模型椎體骨髓脂肪含量的可行性，為探索糖尿病骨髓微血管病變的脂肪-血流調(diào)控機(jī)制奠定技術(shù)基礎(chǔ)。

1　材料與方法

1.1兔糖尿病模型的建立

動(dòng)物實(shí)驗(yàn)經(jīng)武漢大學(xué)醫(yī)院倫理委員會(huì)審查通過。武漢大學(xué)動(dòng)物實(shí)驗(yàn)中心提供3月齡健康新西蘭雄性大白兔12只，空腹1.5～2.0 kg，平均(1.7±0.2) kg。實(shí)驗(yàn)動(dòng)物由武漢大學(xué)人民醫(yī)院實(shí)驗(yàn)動(dòng)物中心單籠飼養(yǎng)，室溫控制在25℃。12只兔適應(yīng)性飼養(yǎng)一周后，測量空腹血糖，12只兔血糖均在正常水平且無明顯差異[(5.5±0.5) mmol/L]。

12只兔禁食、水8 h后，隨機(jī)將兔分為實(shí)驗(yàn)組(A組)6只、對(duì)照組(B組)6只。將四氧嘧啶(Sigma公司)用生理鹽水配制成2.5%溶液，按照100 mg/kg 于30 s內(nèi)由耳緣靜脈攝入實(shí)驗(yàn)組兔體內(nèi)，對(duì)照組給予注射生理鹽水，之后自由進(jìn)食、進(jìn)水。24 h內(nèi)用血糖儀(強(qiáng)生PEB003006P)每小時(shí)監(jiān)測末梢血糖一次。對(duì)于血糖低于2.0 mmol/L或出現(xiàn)嗜睡、不進(jìn)食、驚厥、尖叫等低血糖癥狀的大白兔，經(jīng)耳緣靜脈給予葡萄糖。48 h后，測量外周血糖濃度。單次外周血糖測量值大于14 mmol/L或兩次測量大于11 mmol/L被認(rèn)定為造模成功[9]。若對(duì)于48 h后，實(shí)驗(yàn)組白兔血糖仍正常，補(bǔ)加50 mg/kg四氧嘧啶，直至血糖達(dá)上述標(biāo)準(zhǔn)；對(duì)于血糖大于30 mmol/L兔，肌注長效胰島素，將血糖控制在30 mmol/L以下。

1.2影像設(shè)備及成像技術(shù)

實(shí)驗(yàn)組兔分別于造模成功后0、4、8、12、16周經(jīng)耳緣靜脈注射15 g/L戊巴比妥鈉(2 ml/kg)麻醉。麻醉后將兔仰臥位，足先進(jìn)固定于8通道膝關(guān)節(jié)專用相控陣線圈，運(yùn)用3.0 T超導(dǎo)MR機(jī)(Discovery MR750 Plus，GE Healthcare)行常規(guī)腰椎矢狀位FSE-T1WI、FSE-T2WI和IDEAL-IQ掃描。

矢狀位T1WI掃描參數(shù)：TR 400 ms，TE 13 ms，掃描層厚 3 mm，視野16 cm×16 cm，矩陣512×512，激勵(lì)次數(shù)為1，掃描時(shí)間 2 min20 s。

矢狀位T2WI掃描參數(shù)：TR 2500 ms，TE 102.9 ms，掃描層厚 3 mm，視野16 cm×16 cm，矩陣512×284，激勵(lì)次數(shù)為1，掃描時(shí)間 3 min 25 s。

IDEAL-IQ參數(shù)：翻轉(zhuǎn)角6°，TR 19.6 ms，TE 1.2 ms、3.2 ms、5.2 ms、7.2 ms、9.2 ms、11.2 ms。帶寬125 kHz，掃描層厚3 mm，視野16 cm×12.8 cm，矩陣288×288，激勵(lì)次數(shù)為2，掃描時(shí)間 4 min21 s。

1.3IDEAL-IQ骨髓脂肪含量百分比測定

IDEAL-IQ掃描圖像傳入AW4.6工作站(GE Healthcare)，在造模成功0、4、8、12、16周，由同一研究者選取Fat Fraction像椎體中心層面，對(duì)糖尿病組與對(duì)照組的兔腰3～7椎體勾畫感興趣區(qū)(region of interest，ROI)，勾畫ROI時(shí)，避開椎體頭尾側(cè)的終板軟骨和椎體前后緣骨皮質(zhì)。系統(tǒng)自動(dòng)生成所畫區(qū)域的脂肪含量比值(FF%)。每1個(gè)椎體脂肪百分比測量3次，取平均值記為椎體脂肪含量百分比(圖1)。

1.4骨髓脂肪含量組織病理學(xué)檢查

在第16周完成檢查后，采取空氣栓塞法處死12只兔，取腰3～7椎體用10%多聚甲醛固定，脫鈣兩周，石蠟包埋，沿椎體短軸位切4μm厚薄片，行HE染色。骨髓中脂肪細(xì)胞數(shù)目計(jì)數(shù)由人工完成。在顯微鏡(OLYMPUS BX51)下拍片，隨機(jī)選取3個(gè)相互不連續(xù)的區(qū)域，分別于高倍鏡(×400)視野下統(tǒng)計(jì)脂肪細(xì)胞數(shù)目。取平均值為脂肪細(xì)胞計(jì)數(shù)。

1.5統(tǒng)計(jì)學(xué)分析

采用SPSS 16.0統(tǒng)計(jì)軟件，在實(shí)驗(yàn)組造模成功后對(duì)各時(shí)間點(diǎn)IDEAL-IQ測量所得的實(shí)驗(yàn)組與對(duì)照組腰椎體骨髓脂肪比進(jìn)行重復(fù)測量的方差分析。IDEAL-IQ測量腰椎體脂肪比參數(shù)與HE切片鏡下脂肪細(xì)胞計(jì)數(shù)進(jìn)行Pearson相關(guān)分析，所有結(jié)果以P ＜0.05為差異具有統(tǒng)計(jì)學(xué)意義。

圖1　實(shí)驗(yàn)組兔腰椎常規(guī)MRI和IDEAL-IQ。A：矢狀位T2WI像，黑色箭頭所指為兔腰7椎體；B：矢狀位T1WI像，黑色箭頭所指為兔腰7椎體；C：矢狀位Fat Fraction像，紅色區(qū)域?yàn)楣串嫷挠糜跍y量椎體脂肪含量比的興趣區(qū) 圖2 A：對(duì)照組16周兔椎體骨髓HE染色( ×400)；B：實(shí)驗(yàn)組16周兔椎體骨髓HE染色( ×400)，脂肪細(xì)胞(紅色箭頭)數(shù)量及體積明顯多于對(duì)照組，骨髓細(xì)胞(藍(lán)色箭頭)數(shù)量明顯少于對(duì)照組Fig. 1 A rabbit in the alloxan-induced diabetic group at the week of 16. A: The sagittal T2-weighted image of the rabbit, black arrow refers to L7; B: The sagittal T1-weighted image of the rabbit, black arrow refers to L7; C: The sagittal Fat Fraction image, the red area is the ROI used to measure the fat content of the vertebral body. Fig. 2 A: Bone marrow HE staining in the control group rabbit at the week of 16 （ ×400）； B: Bone marrow HE staining in alloxaninduced diabetic group rabbit at the week of 16 ( ×400）. The amount and volume of the fat cell （red arrow） in alloxan-induced diabetic group are more than the control. The bone marrow cells (blue arrow) reduced in alloxan-induced diabetic group rabbit contrasted to the control.

2　結(jié)果

16周實(shí)驗(yàn)組兔腰椎常規(guī)矢狀位T1WI和T2WI顯示諸腰椎椎體信號(hào)輕度增高。常規(guī)HE染色顯示，16周糖尿病組兔椎體終板下骨髓腔脂肪含量較對(duì)照組明顯增多，骨髓細(xì)胞明顯減少(圖2)。

糖尿病組各時(shí)間節(jié)點(diǎn)兔椎體脂肪含量比服從正態(tài)分布，且組間數(shù)據(jù)方差齊。球形檢驗(yàn)結(jié)果P＞0.05，符合F-H條件，采用重復(fù)測量資料的方差分析。實(shí)驗(yàn)組各時(shí)間點(diǎn)IDEAL-IQ測量椎體骨髓脂肪含量百分比的差異具有統(tǒng)計(jì)學(xué)意義(F=50.387，P ＜0.01)。進(jìn)一步對(duì)各時(shí)間點(diǎn)的脂肪比參數(shù)進(jìn)行兩兩比較，IDEAL-IQ測量實(shí)驗(yàn)組16周椎體脂肪含量百分比與0、4、8、12周差異存在明顯統(tǒng)計(jì)學(xué)意義(表1)。16周實(shí)驗(yàn)組與對(duì)照組的FF值差異有統(tǒng)計(jì)學(xué)意義(t=-10.726，P＜0.05)，見圖3。對(duì)照組的各時(shí)間節(jié)點(diǎn)椎體脂肪含量比服從正態(tài)分布，且組間數(shù)據(jù)方差齊。對(duì)照組的各時(shí)間節(jié)點(diǎn)椎體脂肪比差異無明顯統(tǒng)計(jì)學(xué)意義(F=1.477，P＞0.05)。

16周椎體骨髓脂肪含量比參數(shù)近似正態(tài)分布，Pearson相關(guān)分析結(jié)果顯示IDEAL-IQ測量脂肪含量比與病理脂肪細(xì)胞計(jì)數(shù)呈顯著正相關(guān)關(guān)系(r=0.925，P＜0.05)，見圖4。

3　　討論

本實(shí)驗(yàn)結(jié)果顯示糖尿病兔椎體骨髓脂肪含量比值在第16周時(shí)較0、4、8和12周明顯增高，IDEAL-IQ測量骨髓含量與組織病理脂肪細(xì)胞計(jì)數(shù)具有高度相關(guān)性，顯示IDEAL-IQ技術(shù)活體測量糖尿病骨髓脂肪含量是可行的。

圖3　各時(shí)間點(diǎn)糖尿病組與對(duì)照組IDEAL-IQ測量兔椎體骨髓脂肪比例的比較　圖4　IDEAL-IQ測量脂肪含量比與病理脂肪細(xì)胞計(jì)數(shù)的相關(guān)性Fig. 3 Comparison of bone marrow fat fraction with IDEAL-IQ between the diabetes group and the control group rabbits at each time point.Fig.4 Correlation between fat content and the amount of the fat cells

表1　糖尿病組、對(duì)照組各時(shí)間點(diǎn)IDEAL-IQ椎體脂肪比的比較(%)Tab. 1 Comparison of IDEAL-IQ vertebral body fat content between the diabetic group and the control group at each time point (%)

正常機(jī)體骨髓葡萄糖的代謝是肌肉組織的兩倍[10]。糖尿病由于胰島素的缺乏，機(jī)體糖代謝的紊亂會(huì)導(dǎo)致椎體骨髓的脂肪堆積，而堆積的反式脂肪酸會(huì)反過來抑制骨髓葡萄糖的代謝[11]。另一方面，由于骨髓脂肪細(xì)胞的填充，能夠代謝葡萄糖的骨髓細(xì)胞減少，骨髓微環(huán)境的糖代謝進(jìn)一步減弱。研究表明，同一機(jī)體不同椎體之間或者不同個(gè)體的椎體脂肪含量由于性別、年齡、疾病等因素也會(huì)存在差異[12]。糖尿病、肥胖以及年齡的增長會(huì)導(dǎo)致骨髓脂肪含量的增加[6, 13-14]。而椎體骨髓脂肪化與骨質(zhì)疏松、椎間盤退變關(guān)系密切[10, 15-16]，糖尿病患者的椎體脂肪化是椎體骨質(zhì)疏松、椎間盤退變發(fā)生的早期重要表現(xiàn)。Sakellaridis N[15]在對(duì)臨床椎間盤手術(shù)病人的回顧性分析中發(fā)現(xiàn)，糖尿病患者發(fā)生重度椎間盤退變的概率更大；Ville Huovinen[10]運(yùn)用高分辨率多魔角離體波譜對(duì)豬糖尿病椎體的脂肪含量進(jìn)行了定量分析，同時(shí)論證了葡萄糖代謝與椎體脂肪含量呈負(fù)相關(guān)關(guān)系。本實(shí)驗(yàn)結(jié)果顯示骨髓脂肪含量可能可以作為糖尿病骨髓病變的影像學(xué)生物標(biāo)志物。

IDEAL-IQ技術(shù)利用“混合型水脂分離算法”對(duì)多回波復(fù)數(shù)數(shù)據(jù)進(jìn)行重建、整合，最終計(jì)算出組織脂肪比[17]。Ideal-IQ技術(shù)結(jié)合非對(duì)稱采集技術(shù)與迭代最小二乘水脂分離算法，利用3D FSPGR在一個(gè)TR中采集6個(gè)梯度回波，利用fiy-back方法進(jìn)行k空間填充。相對(duì)于傳統(tǒng)IDEAL技術(shù)[18]，IDEAL-IQ用時(shí)短，一次掃描可以產(chǎn)生6幅圖像，分別是fat、water、in-phase、out-phase、R2*maps 和fat fraction maps。IDEAL-IQ所產(chǎn)生的fat fraction maps可以直接由計(jì)算出骨髓感興趣區(qū)內(nèi)的脂肪含量百分比。該方法由于無創(chuàng)、可重復(fù)性好，可以對(duì)椎體脂肪含量的變化進(jìn)行定量評(píng)價(jià)，進(jìn)而客觀反映骨髓代謝功能的變化。Ergen FB[19]首次采用IDEAL-IQ技術(shù)顯示女性椎體骨密度和椎體脂肪含量存在負(fù)相關(guān)。Anne[7]在利用活體波譜和水脂分離脂肪定量技術(shù)研究骨質(zhì)疏松與椎體脂肪含量關(guān)系時(shí)發(fā)現(xiàn)，這兩種技術(shù)在評(píng)價(jià)椎體脂肪含量方面具有高度一致性。而Jens-Peter Kühn[8]論證經(jīng)過T2*衰減的修正和脂肪的多譜峰分布的水脂分離技術(shù)對(duì)于評(píng)估骨質(zhì)疏松患者腰椎椎體脂肪含量具有更高的診斷效能。本研究首次探索IDEAL-IQ運(yùn)用于糖尿病兔椎體脂肪比的定量研究，結(jié)果顯示IDEAL-IQ可以便捷、有效、動(dòng)態(tài)檢測糖尿病骨髓脂肪含量的變化，為揭示早期糖尿病骨髓病變以脂肪代謝為中心的病理生理機(jī)制以及未來相關(guān)臨床藥物治療效果的評(píng)估提供了影像學(xué)證據(jù)。

本研究的局限性：(1)本研究實(shí)驗(yàn)組兔血糖水平維持在(14±2) mmol/L，且實(shí)驗(yàn)組兔血糖波動(dòng)幅度小，糖尿病兔椎體脂肪化程度、進(jìn)展速度與血糖濃度水平以及波動(dòng)情況的相關(guān)性有待進(jìn)一步確認(rèn)；(2)IDEAL-IQ技術(shù)僅是骨髓組織脂肪比例的定量研究，下一步需要離體骨髓標(biāo)本高分辨率波譜或質(zhì)譜分析深入研究脂肪酸成分的變化；(3)本研究實(shí)驗(yàn)樣本較小，欲探索糖尿病椎體骨髓脂肪變化詳細(xì)機(jī)制，仍需后續(xù)大樣本實(shí)驗(yàn)研究證實(shí)。另外，兔糖尿病椎體骨髓脂肪化特點(diǎn)是否與人體椎體相一致，仍需后續(xù)臨床研究進(jìn)一步證實(shí)?？傊?，IDEAL-IQ定量評(píng)估兔糖尿病模型椎體骨髓脂肪含量是可行的。

［References］

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資訊 Information

The feasibility of IDEAL-IQ quantitative evaluation of vertebral fat fraction content in rabbit models of diabetes mellitus

HU Lei, ZHA Yun-fei*, LIN Yuan, XING Dong, GONG Wei, WANG Ke-jun, YAN Liyong, WANG Jiao

Department of Radiology， Renmin Hospital of Wuhan University， Wuhan 430060，China

*Correspondence to: Zha YF, E-mail: zhayunfei999@126.com

11 Sep 2015, Accepted 20 Oct 2015

Diabetes mellitus， Experimental； Vertebral marrow； Quantification； Magnetic resonance imaging； Laboratory animal science; Rabbits

湖北省自然科學(xué)基金項(xiàng)目(編號(hào)：2013CFB242)；湖北省衛(wèi)生廳科研資助項(xiàng)目(編號(hào)：JX6B68)

武漢大學(xué)人民醫(yī)院放射科，武漢430060

查云飛，E-mail：zhayunfei999@126. com

2015-09-11

R445.2；R-332

A

10.3969/j.issn.1674-8034.2015.12.012

接受日期：2015-10-20

胡磊, 查云飛, 林苑, 等. IDEAL-IQ定量評(píng)價(jià)兔糖尿病模型椎體骨髓脂肪含量的可行性研究. 磁共振成像, 2015, 6(12): 941-946.

ACKNOWLEDGMENTS This work was part of natural science foundation of Hubei province （ No. 2013CFB242） and scientific research project of health department of Hubei (No. JX6B68).

Abrtract Objective: To use the IDEAL-IQ technique to estimate vertebral fat fraction(FF) in alloxan-induced diabetic rabbits. Materials and Methods: Twelve young New Zealand white rabbits were randomly assigned to alloxan-induced diabetic group(n=6) and control group(n=6). The rabbits in alloxan-induced diabetic group were injected with a total amount of 100 mg/kg of alloxan. Both of the rabbits in alloxaninduced diabetic and control group underwent magnetic resonance imaging (TIWI, T2WI， IDEAL-IQ） at each time point（0， 4， 8， 12， 16 weeks）. Each vertebral fat fraction was measured at a standard workstation （AW 4.6； GE Medical Systems）. Region of interest (ROI) had a shape of rectangle and they were drawn manually. HE staining was performed. Results: Slight increase of the signal of the lumbar vertebral bodies was found at the T1WI and T2WI in the alloxan-induced diabetic group at the week of 16. Compared to the control group, the alloxan-induced diabetic group showed thereduce of bone cells and increase of the fat cells. The alloxan-induced diabetic group has statistically differences in vertebral fat fraction at each time point(F=50.387，P＜0.01). The control group has no statistical differences in vertebral fat fraction at each time point(F=1.477，P＞0.05). There is statistical difference in vertebral fat fraction between alloxan-induced diabetic and control group at the week of 16(t=-10.726, P＜0.05）. A significant positive correlation is found between vertebral fat fraction and fat cell count(r=0.925, P＜0.05). Conclusion: IDEAL-IQ technique can quantify the vertebral fat fraction in alloxan-induced diabetic rabbits.