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临床研究
MRI基本征象结合ADC值鉴别垂体大腺瘤和鞍区脑膜瘤
韩涛 张婧 王丹 张斌 邓靓娜 林晓强 景梦园 周俊林

Cite this article as: Han T, Zhang J, Wang D, et al. Differential diagnosis of pituitary macroadenomas and sellar meningiomas by MRI basic signs combined with ADC value[J]. Chin J Magn Reson Imaging, 2021, 12(5): 6-11.本文引用格式:韩涛, 张婧, 王丹, 等. MRI基本征象结合ADC值鉴别垂体大腺瘤和鞍区脑膜瘤[J]. 磁共振成像, 2021, 12(5): 6-11. DOI:10.12015/issn.1674-8034.2021.05.002.


[摘要] 目的 探讨MRI基本征象结合ADC值鉴别诊断垂体大腺瘤和鞍区脑膜瘤的价值。材料与方法 回顾性分析经病理证实的42例垂体大腺瘤和40例鞍区脑膜瘤,所有病例术前行磁共振成像(magnetic resonance imaging,MRI)和扩散加权成像(diffusion-weighted imaging,DWI)检查,并在肿瘤实体部分测量表观扩散系数(apparent diffusion coefficient,ADC)值,与病理结果比较分析。统计学方法使用t检验、卡方检验,并用受试者工作特征(receiver operating characteristic,ROC)曲线评估各参数鉴别两组肿瘤的诊断效能。结果 垂体大腺瘤和鞍区脑膜瘤间,明显强化(33%/95%,χ2=33.581)、束腰征(93%/7.5%,χ2=50.831)、包绕颈内动脉(95%/57.5%,χ2=16.390)、蝶鞍扩大(93%/52.5%,χ2=16.998)、垂体不能辨认(95%/47.5%,χ2=23.135)和垂体柄不可见(90%/62.5%,χ2=7.761),均具有统计学意义(P<0.05)。垂体大腺瘤和鞍区脑膜瘤的ADCmax (ADCmean和ADCmin)分别为(1.126±0.266)×10-3 mm2/s和(0.855±0.176)×10-3 mm2/s [(1.052±0.271)×10-3 mm2/s和(0.817±0.177)×10-3 mm2/s,(0.971±0.288)×10-3 mm2/s和(0.777±0.182)×10-3 mm2/s),P<0.001]。在ADC值中,ADCmax诊断效能最优,AUC值为0.877 (95% CI,0.791~0.962),当ADCmax阈值为0.970 × 10-3 mm2/s时,鉴别二者的敏感度、特异度分别为81%、92.5%。结论 MRI基本征象结合ADC值对垂体大腺瘤和鞍区脑膜瘤有较高的临床诊断价值,可提高术前诊断准确率。
[Abstract] Objective To explore the value of MRI signs combined with ADC value in the differential diagnosis of pituitary macroadenomas and sellar meningiomas. Materials andMethods Forty-two cases of pituitary macroadenomas and 40 cases of sellar meningiomas confirmed by pathology, were analyzed retrospectively. All cases were examined by traditional magnetic resonance imaging (MRI) and diffusion-weighted imaging (DWI) before operation.The apparent diffusion coefficient (ADC) value was measured in the solid part of the tumor and compared with the results of pathological diagnosis. t-test, Chi-square test were used in statistical methods, and the diagnostic efficacy of each parameter in differentiating the two groups of tumors was evaluated by the receiver working characteristic (ROC) curve.Results Between pituitary macroadenomas and sellar meningiomas, significant enhancement (33%/95%, χ2=33.581), waist sign (93%/7.5%, χ2=50.831), wrapped around internal carotid artery (95%/57.5%, χ2=16.390), enlarged sella turcica (93%/52.5%, χ2=16.998), pituitary unrecognizable (95%/47.5%, χ2=23.135) and pituitary stalk invisible (90%/62.5%, χ2=7.761) were statistically significant (P<0.05). The ADCmax (ADCmean and ADCmin) of pituitary macroadenoma and sellar meningioma was (1.126±0.266)×10-3 mm2/s and (0.855±0.176)×10-3 mm2/s [(1.052±0.271)×10-3 mm2/s and (0.817±0.177)×10-3 mm2/s, (0.971±0.288)×10-3 mm2/s and (0.777±0.182)×10-3 mm2/s, P<0.001]. Among ADC values, ADCmax demonstrated good performance with an AUC of 0.877 (95% CI, 0.791—0.962) and when the cut-off of ADCmax is 0.970×10-3 mm2/s, the sensitivity and specificity of distinguishing them are 81% and 92.5%.Conclusions The basic signs of MRI combined with ADC value have high clinical value in the diagnosis of pituitary macroadenomas and sellar meningiomas, Which can improve the accuracy of preoperative diagnosis.
[关键词] 垂体大腺瘤;鞍区脑膜瘤;磁共振成像;扩散加权成像;表观扩散系数
[Keywords] pituitary macroadenomas;sellar meningiomas;magnetic resonance imaging;diffusion-weighted imaging;apparent diffusion coefficient

韩涛 1, 2, 3   张婧 1, 2, 3   王丹 1, 3   张斌 1, 2, 3   邓靓娜 1, 2, 3   林晓强 1, 2, 3   景梦园 1, 2, 3   周俊林 1, 3*  

1 兰州大学第二医院放射科,兰州 730030

2 兰州大学第二临床医学院,兰州 730030

3 甘肃省医学影像重点实验室,兰州 730030

周俊林,E-mail:lzuzjl601@163.com

全体作者均声明无利益冲突。


基金项目: 国家自然科学基金面上项目 81772006 兰州大学第二医院“萃英科技创新计划”应用基础研究项目 CY2017-MS03
收稿日期:2020-11-13
接受日期:2021-01-21
DOI: 10.12015/issn.1674-8034.2021.05.002
本文引用格式:韩涛, 张婧, 王丹, 等. MRI基本征象结合ADC值鉴别垂体大腺瘤和鞍区脑膜瘤[J]. 磁共振成像, 2021, 12(5): 6-11. DOI:10.12015/issn.1674-8034.2021.05.002.

       垂体瘤约占颅内肿瘤10%~15%,是颅内常见肿瘤之一。垂体大腺瘤是指直径大于10 mm的腺瘤,具有多方向生长的特点[1]。鞍区脑膜瘤约占脑膜瘤的5%~10%,局部解剖复杂,肿瘤常与海绵窦、颈内动脉、视神经等关系密切,手术难度大[2]。当脑膜瘤向鞍内生长,垂体大腺瘤向上生长并向周围蔓延,尤其是无功能垂体大腺瘤时,两者的MRI征象存在一定重叠,不易鉴别,而两者手术入路不同,脑膜瘤一般需开颅手术,垂体大腺瘤一般经鼻-蝶窦手术[3, 4, 5]。本研究通过对比分析垂体大腺瘤和鞍区脑膜瘤的MRI征象、ADC值,期望可以对二者进行仔细的术前评估,提高诊断准确率,从而选择合适的手术入路,有效地提高显微手术效果。

1 材料与方法

1.1 一般资料

       回顾性收集2014年1月至2019年3月我院经手术病理证实的42例垂体大腺瘤及同期经手术病理证实的40例鞍区脑膜瘤。垂体大腺瘤中男25例,女17例,年龄29~80岁,平均年龄51.9岁。鞍区脑膜瘤中男7例,女33例,年龄31~66岁,平均年龄51.35岁。本研究经过本单位医学伦理委员会批准(批准文号:2020A-109),免除受试者知情同意。

1.2 仪器与方法

       采用Siemens 3.0 T Verio MR扫描仪,82例患者均于术前接受T1WI、T2WI、T2-FLAIR、DWI及MR增强扫描。扫描序列及参数:GRE:T1WI (TR 550 ms,TE 11 ms),层厚5.0 mm,层间距1.5 mm,视野(FOV) 260 mm×260 mm,矩阵256×256;TSE:T2WI (TR 2200 ms,TE 96 ms),回波时间10 ms,回波链长度8,激励次数2。T2WI-FLAIR:(TR 9000 ms,TE 110.0 ms),层厚5.0 mm,层间距1.5 mm;DWI (SEEPI序列):加频率选择脂肪抑制技术,(TR 4000 ms,TE 100 ms),层厚9 mm,层间距1 mm,FOV 260 mm×260 mm,矩阵256×192,在x、y、z轴3个方向上施加扩散梯度(b值=0、1000 s/mm²)。对比剂为Gd-DTPA 0.1 mmol/kg体质量,流率3 mL/s,获得轴位、矢状位和冠状位增强T1WI。

1.3 图像分析与测量

       采用Philips R2.6.3.1工作站进行图像后处理,重建ADC图,由2名从事神经影像MRI诊断工作并具有15年以上经验丰富的影像诊断医师以盲法独立观察图像至少2次,间隔时间1周之内,如有分歧经协商后达成一致。观察并记录肿瘤信号特点、强化程度、束腰征、蝶鞍扩大、脑膜尾征、包绕颈内动脉、是否可见垂体柄及垂体是否能辨认的影像特征。根据T1WI、T2WI以及增强图像确定病变实性成分,于重建ADC图上尽量避开病灶内肉眼所见的囊变、坏死及出血区,在每个层面手动绘制3个椭圆形ROI,面积为20~30 mm2,分别测量每个ROI的ADCmean、ADCmin及ADCmax,然后计算两位神经影像医生测量的ADCmax、ADCmean和ADCmin的平均值。

1.4 病理检查

       所有手术切除的肿瘤所得标本用4%的福尔马林固定24 h,常规脱水,石蜡包埋,切取4.0 μm厚石蜡切片,进行HE染色和免疫组化染色,免疫组织化学采用EnVision两步法染色。脑膜瘤用EMA对肿瘤细胞进行标记,细胞浆或细胞膜呈棕黄色为阳性。垂体大腺瘤用免疫组化检查GH、PRL、ACTH、TSH、FSH、LH的表达情况,免疫组化切片上见垂体瘤细胞浆着黄色或棕黄色为阳性细胞,阳性细胞数>5%为分泌相应激素的腺瘤,若垂体细胞包浆未着色或阳性细胞数<5%,则为无分泌激素的腺瘤。

1.5 统计学分析

       采用SPSS 23.0统计分析软件,经正态分布检验后,垂体大腺瘤和鞍区脑膜瘤常规MRI表现比较采用卡方检验,ADC值比较采用独立样本t检验,年龄等计量资料采用x¯±sP<0.05有统计学意义。并绘制ROC曲线,分析垂体大腺瘤与鞍区脑膜瘤的最佳诊断阈值及相应敏感度与特异度。

2 结果

2.1 两组肿瘤临床表现

       42例垂体大腺瘤中,视力下降者3例,头痛、头晕者5例,眼睑下垂者7例,闭经者9例,泌乳者8例,肢端肥大者4例,其他表现者6例。40例鞍区脑膜瘤中,头痛、头晕者6例,视力下降、模糊者18例,头痛伴视力下降者13例,闭经者1例,泌乳者2例。两组患者的年龄差异无统计学意义,P>0.05。

2.2 两组肿瘤的MRI基本征象

       42例垂体大腺瘤中,T1WI呈低信号,T2WI呈中等偏高信号。5例瘤内发生坏死囊变,囊变部分T1W1呈低信号,T2WI呈高信号;4例瘤内出血,TIWl及T2WI均呈不均匀高信号;增强扫描轻中度强化28例,瘤内出血坏死囊变时不均匀强化;本组中90%的肿瘤较大,突破鞍隔向上生长,压迫视交叉,使垂体柄受压移位,甚至显示不清,且包绕两侧颈内动脉和海绵窦40例,形成较典型的“束腰征”39例(图1)。40例鞍区脑膜瘤中,肿瘤实性部分未见明显出血,T1WI显示较低信号,T2WI呈中等或稍高信号,增强后肿瘤明显均匀强化38例,邻近脑膜明显增厚并强化25例,即“脑膜尾征”(图2)。其影像征象如表1所示。

图1  女,62岁,垂体大腺瘤。A、B:鞍区可见类圆形长T1、长T2信号影,信号均匀,边界清楚;C:DWI呈高信号;D:ADC呈低信号;E、F:增强扫描病灶呈不均匀强化;G:病理结果(HE ×100),镜下见瘤组织之瘤细胞弥漫分布,细胞大小、形态一致,胞核小,圆形,核染色质均匀,核分裂象少见,间质血管丰富。H:免疫组化( ×200)示胞浆呈棕褐色,syn表达强阳性
图2  男,55岁,过渡型脑膜瘤。A、B:鞍区见不规则形占位,T1WI呈较低信号,T2WI呈较高信号,边界不清;C:DWI呈高信号;D:ADC低信号;E、F:增强扫描肿瘤区域强化显著且均匀。G:病理结果(HE ×100),镜下见瘤组织之瘤细胞由脑膜皮及纤维细胞构成,束状、旋涡状排列,椭圆形、卵圆形、长杆状,无明显异型性,核分裂象少见,间质伴慢性炎细胞浸润。H:EMA ( ×200)示胞浆棕褐色染色,肿瘤来源于上皮
Fig. 1  Female, 62 years old, pituitary macroadenoma. A, B: There were round-like long T1 and long T2 signals in the sellar region, with uniform signal and clear boundary. C: DWI showed high signal. D: ADC showed low signal. E, F: The solid part of tumor showed inhomogeneous enhancement. G: pathological results (HE×100), microscopically, the tumor cells were diffusely distributed, the size and shape of the cells were the same, the nucleus was small and round, the nuclear chromatin was uniform, mitosis was rare, and the interstitial vessels were abundant. H: immunohistochemical staining ( ×200) showed brown cytoplasm and strong positive expression of syn.
Fig. 2  Male, 55 years old, transitional meningioma. A, B: There was irregular space-occupying in the sellar region, with low signal on T1 and high signal on T2, and the boundary was unclear. C: DWI showed high signal. D: ADC showed low signal, E, F: Significant and even enhancement in enhanced scan. G: Pathological results (HE×100), the tumor cells in the tumor tissue were composed of meningeal skin and fibrous cells, arranged in bundles and swirls, oval, oval and long rod, without obvious atypia, mitosis was rare, and stroma was associated with chronic inflammatory cell infiltration. H: EMA ( ×200) showed brown staining in the cytoplasm and the tumor originated from the epithelium.
表1  垂体大腺瘤与鞍区脑膜瘤MRI基本征象对比
Tab. 1  Comparison of MRI basic signs between pituitary macroadenomas and sellar meningiomas

2.3 两组肿瘤的DWI信号强度及ADC值对比分析

       在42例垂体大腺瘤中,肿瘤实体成分在DWI上19例呈高或稍高信号,15例呈等信号,8例呈低信号;ADCmax、ADCmean和ADCmin分别为(1.126±0.266)×10-3 mm2/s、(1.052±0.271)×10-3 mm2/s和(0.971± 0.288)×10-3 mm2/s。在40例鞍区脑膜瘤中,肿瘤实体成分在DWI上22例呈高或稍高信号,15例呈等信号,3例呈低信号。两组肿瘤DWI信号强度比较无统计学意义(P>0.05) (表1);ADCmax、ADCmean和ADCmin分别为(0.855±0.176)×10-3 mm2/s、(0.817±0.177)×10-3 mm2/s和(0.777±0.182)×10-3 mm2/s,均小于垂体大腺瘤。两组肿瘤实性成分ADCmax值、ADCmin值、ADCmean值比较差异具有统计学意义(P<0.001) (表2图3)。

图3  ADCmean值、ADCmin值及ADCmax值鉴别诊断垂体大腺瘤与鞍区脑膜瘤的ROC曲线
Fig. 3  ROC curve of pituitary macroadenomas and Sellar meningiomas for differential diagnosis of ADCmin value, ADCmin value and ADCmax value.
表2  垂体大腺瘤与鞍区脑膜瘤ADC值对比
Tab. 2  Comparison of ADC values between pituitary macroadenomas and sellar meningiomas

2.4 MRI基本征象、MRI基本征象结合ADC值与病理诊断垂体大腺瘤和鞍区脑膜瘤的情况比较

       MRI基本征象诊断垂体大腺瘤和鞍区脑膜瘤的准确率分别为76.19% (32/42)、82.5% (33/40),DWI结合ADC值诊断垂体大腺瘤和鞍区脑膜瘤的准确率分别为95.24% (40/42)、92.5% (37/40) (表3)。

表3  MRI基本征象、MRI基本征象结合ADC值与病理诊断垂体大腺瘤和鞍区脑膜瘤情况(例)
Tab. 3  Basic signs of MRI and MRI combined with ADC value and pathology in the diagnosis of pituitary macroadenomas and sellar meningiomas (n)

3 讨论

3.1 总结

       鞍区脑膜瘤起源于邻近的硬脑膜表面,包括鞍结节、鞍隔及垂体窝周围的硬脑膜等[6]。鞍区脑膜瘤和垂体大腺瘤是鞍区常见的肿瘤,多为良性肿瘤,但部分肿瘤较大时呈浸润性生长,可包绕或侵犯周围邻近组织,增加了手术难度及复发率[7]。Wu等[8]发现定量双能CT成像、碘含量、Hu曲线斜率和平均CT值可作为鞍区脑膜瘤和垂体腺瘤鉴别诊断的指标。MRI是颅内肿瘤的常用检查方法[9],但是在常规MRI上,垂体大腺瘤与鞍区脑膜瘤的表现存在一定交叉,术前误诊率较高,而二者的手术入路又不同,因此,术前鉴别垂体大腺瘤和鞍区脑膜瘤尤为重要。

       有研究报道[10, 11, 12],ADC值在脑肿瘤的鉴别中起着重要作用,包括良性脑膜瘤、不典型脑膜瘤、恶性脑膜瘤和孤立性纤维性脑膜瘤,很少有研究用ADC值鉴别垂体大腺瘤与鞍区脑膜瘤。基于以上背景,笔者推测MRI基本征象结合ADC值可以较好地鉴别鞍区脑膜瘤与垂体大腺瘤。本研究回顾分析经手术病理证实的42例垂体大腺瘤和40例鞍区脑膜瘤的MRI基本征象,并对其DWI信号和ADC值进行分析,结果发现ADC值有助于二者的鉴别诊断。

3.2 常规MRI表现分析

       本研究中,37例鞍区脑膜瘤以头痛、视力下降为主要临床表现,21例垂体大腺瘤以闭经、泌乳为首发症状,与文献报道一致[4]。鞍区脑膜瘤与垂体大腺瘤不同的病理生理改变决定了其影像特点。本研究中垂体大腺瘤T2WI高信号占比高于鞍区脑膜瘤,二者间具有统计学意义,可能是由于垂体大腺瘤肿瘤内部较鞍区脑膜瘤易发生坏死、出血及囊变。有研究发现鞍区脑膜瘤强化比率较垂体大腺瘤大,且强化显著而均匀[13],和本组结果一致,这与鞍区脑膜瘤血供丰富,坏死囊变少见,而垂体大腺瘤相对血供不丰富,易坏死囊变出血有关[14]。本研究结果显示垂体大腺瘤束腰征征象占比明显大于鞍区脑膜瘤,这与垂体大腺瘤质地软,肿瘤通过鞍隔生长时受限呈束腰征,而脑膜瘤质地硬,即使在鞍内生长,束腰征也少见,垂体一般可显示有关[15, 16]。本组资料中垂体大腺瘤包绕颈内动脉40例,鞍区脑膜瘤包绕颈内动脉23例,显示了二者的生物行为不同,是因为垂体大腺瘤侵袭性强,易侵犯邻近骨质、包绕颈内动脉,而鞍区脑膜瘤匍匐生长,只有生长到颈内动脉处才能包饶。本研究发现垂体大腺瘤蝶鞍扩大占比高于鞍区脑膜瘤,可能是因为鞍区脑膜瘤受鞍隔阻挡,主要向鞍上生长,较少突破鞍隔向下延伸,蝶鞍扩大并不明显,而垂体大腺瘤首先在鞍内生长,使蝶鞍球形扩大,鞍底下陷进而突破鞍隔,延伸到鞍上,与文献报道[16]相符。本组资料中,62.5% (25/40)的鞍区脑膜瘤可见脑膜尾征,与其病理基础肿瘤浸润与邻近脑膜增粗、远端变细有关[17]。40% (17/25)的垂体大腺瘤可见脑膜尾征,可能与垂体大腺瘤较大时刺激邻近脑膜,致其轻度增厚有关,二者间不具有统计学意义。本研究中鞍区脑膜瘤的垂体及垂体柄较垂体大腺瘤清晰可见,这可能与二者的生长方式有关,鞍区脑膜瘤向后生长,垂体柄常受压,部分显示不清,垂体MRI增强扫描仍能辨认;而垂体大腺瘤向上生长,推压垂体柄,使之显示不清,也不存在正常垂体结构,与以往研究一致[18]

3.3 DWI信号强度及ADC值分析

       DWI通过反映组织间水分子弥散情况,提供肿瘤内部微环境信息[19, 20]。本研究中,MRI基本征象结合ADC值诊断垂体大腺瘤和鞍区脑膜瘤的准确率明显高于MRI基本征象(表3),ADC值在两种肿瘤鉴别中有明显统计学意义,而DWI信号在二者间无统计学意义,这可能是由于DWI 信号的影响因素比较多,主要有扩散敏感系数(b)、ADC值、T2穿透效应、各向异性等[21];影响肿瘤ADC值的因素相对较少,包括肿瘤细胞密度、核浆比、肿瘤基质及胞浆内大分子物质含量等。当肿瘤细胞排列紧密、核浆比例高、基质稀少时,水分子扩散受限,DWI信号增高,ADC值较低[22, 23]。本研究中鞍区脑膜瘤的ADCmax、ADCmean和ADCmin值均低于垂体大腺瘤(P<0.001),ADCmax对鉴别垂体大腺瘤和鞍区脑膜瘤的能力相对高于ADCmin和ADCmean,AUC值为0.877 (最佳截断值为0.970×10-3 mm2/s),这些发现与先前的研究结果一致[24],分析其原因可能与细胞类型和核浆比不同有关。垂体大腺瘤内纤维组织增生,疏松排列;而脑膜瘤细胞彼此之间紧密连接,细胞间区域被大量的胞浆与细胞内复杂蛋白分子紧密相连[25],限制了细胞内外水分子的运动。因此,与垂体大腺瘤相比,鞍区脑膜瘤细胞排列紧密,细胞外间隙减小,基质稀少,从而限制了水的扩散。这种组织学差异解释了ADC图上的差异。

       本研究依然存在不足之处,因鞍区脑膜瘤病例数较少,未对鞍区脑膜瘤进行分级,今后可扩大样本量对不同级别的鞍区脑膜瘤进行研究。磁共振成像新技术,如灌注加权成像(PWI)和磁化率加权成像(SWI),不包括在这项研究中,将不得不在未来探索。

       综上所述,垂体大腺瘤和鞍区脑膜瘤的MRI基本征象(T2WI信号、强化特点、束腰征、包绕颈内动脉、碟鞍扩大、是否可见垂体柄、垂体是否能辨认)结合ADC值可以较好地鉴别二者,有助于术前评估、选择合适的手术入路,有效地提高显微手术效果。

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