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临床研究
最小表观弥散系数值鉴别诊断儿童腹膜后外周神经母细胞性肿瘤的价值
任翔 杨秀军

Cite this article as: Ren X, Yang XJ. Differential diagnosis of retroperitoneal peripheral neuroblastic tumors in children by minima apparent diffusion coefficient value of diffusion weighted imaging. Chin J Magn Reson Imaging, 2020, 11(9): 771-775.本文引用格式:任翔,杨秀军.最小表观弥散系数值鉴别诊断儿童腹膜后外周神经母细胞性肿瘤的价值.磁共振成像, 2020, 11(9): 771-775. DOI:10.12015/issn.1674-8034.2020.09.010.


[摘要] 目的 探讨最小表观弥散系数(apparent diffusion coefficient,ADC)值鉴别诊断儿童常见腹膜后外周神经母细胞性肿瘤(peripheral neuroblastic tumors,pNT)的价值。材料与方法 回顾性分析22例手术病理证实的腹膜后神经母细胞性肿瘤的磁共振成像(magnetic resonance imaging ,MRI)资料,所有患儿术前均接受MRI平扫包括弥散加权成像(diffusion weighted imaging,DWI)检查,16例同时行增强扫描。测量肿瘤实质部分的最小ADC值,绘制受试者操作特征曲线(receiver operating characteristic curve,ROC),比较3组腹膜后pNT间的差异。结果 节神经瘤(ganglioneuroma,GN) 5例(22.73%),平均最小ADC值最高,为(1.160±0.310)×10-3 mm2/s;神经母细胞瘤(neuroblastoma,NB) 10例(45.45%),平均最小ADC值最低,为(0.586±0.146)×10-3 mm2/s;节神经母细胞瘤(ganglioneuroblastoma,GNB) 7例(31.82%),平均最小ADC值介于上述两者之间,为(0.794±0.156)×10-3 mm2/s ;3组间差异有统计学意义(F=15.386 ,P=0.000077) ;3组间ROC曲线显示,以0.706×10-3 mm2/s为最小ADC临界值,鉴别诊断节神经瘤和节神经母细胞瘤的敏感度为100%、特异度为50%;以0.665×10-3 mm2/s为最小ADC临界值,鉴别诊断节神经母细胞瘤和神经母细胞瘤的敏感度为87.5%、特异度为80%。结论 最小ADC值在儿童常见3种腹膜后pNT鉴别诊断中具有较高应用价值。
[Abstract] Objective: To evaluate minimal apparent diffusion coefficient (ADC) value in the differential diagnosis of common retroperitoneal peripheral neuroblastic tumors (pNT) in children.Materials and Methods: Magnetic resonance imaging (MRI) findings of 22 children with retroperitoneal pNTs proved by surgery and pathology were retrospectively analyzed, of which, 5 patients (22.73%) were ganglioneuroma (GN), 7 patients (31.82%) ganglioneuroblastoma (GNB), and 10 patients (45.45%) neuroblastoma (NB). All children underwent plain MRI and diffusion weighted imaging (DWI) before surgery, and 16 of them underwent contrast-enhanced scanning. The minimum ADC value of the parenchymal part of the tumor was measured, and their difference between the three was compared and plotted the receiver operating characteristic (ROC) curve to analyze its diagnostic efficacy.Results: The minimum ADC value of GN was the highest [(1.160±0.310)×10-3 mm2/s], and the minimum ADC value of NB was the lowest [(0.586±0.146)×10-3 mm2/s]. The mean ADC value of GNB was between the above two [(0.794±0.156)×10-3 mm2/s]. There was significant difference among the three groups (F=15.386; P=0.000077). After plotting the ROC curves among the three, the results revealed that the sensitivity of differential diagnosis between GN and GNB was 100% and the specificity was 50% taking the minimum ADC value=0.706×10-3 mm2/s as the cut-off value. Taking a cut-off value of minimum ADC value=0.665×10-3 mm2/s, the sensitivity of differential diagnosis between GNB and NB was 87.5% and the specificity was 80%.Conclusions: The minimal ADC value embraces high clinical value in the differential diagnosis of three common retroperitoneal pNT in children.
[关键词] 神经母细胞瘤;腹膜后间隙;磁共振成像;儿童
[Keywords] neuroblastoma;retroperitoneal space;magnetic resonance imaging;child

任翔 上海交通大学附属儿童医院放射科,上海 200062

杨秀军* 上海交通大学附属儿童医院放射科,上海 200062

通信作者:杨秀军,E-mail:yangxj01@shchildren.com

利益冲突:无。


收稿日期:2020-04-25
接受日期:2020-07-25
中图分类号:R445.2; R735.4 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2020.09.010
本文引用格式:任翔,杨秀军.最小表观弥散系数值鉴别诊断儿童腹膜后外周神经母细胞性肿瘤的价值.磁共振成像, 2020, 11(9): 771-775. DOI:10.12015/issn.1674-8034.2020.09.010.

       外周神经母细胞性肿瘤(peripheral neuroblastic tumors ,pNT)是一类起源于原始神经脊外胚层移行细胞的胚胎性肿瘤,主要来源于交感神经节及肾上腺髓质,是儿童最常见的颅外实体肿瘤,腹膜后较多见[1,2]。pNT分为节细胞神经瘤(ganglioneuroma ,GN)、节神经母细胞瘤(ganglioneuroblastoma,GNB),和神经母细胞瘤(neuroblastoma,NB)[3],其中节神经母细胞瘤(GNB)包括混合型节细胞神经母细胞瘤(ganglioneuroblastoma intermixed,GNBi)和结节性节细胞神经母细胞瘤(ganglioneuroblastoma nodular GNBn)。GN为良性肿瘤,NB为高度恶性肿瘤,GNB的恶性程度介于两者之间[4]。肿瘤的预后取决于患儿诊断时的年龄、临床分期、组织学类型,因此早期的定性诊断可以有效指导临床治疗方案的确定,改善患儿的预后效果。本研究通过对比分析儿童常见三种腹膜后pNT的磁共振成像(magnetic resonance imaging,MRI)征象、弥散加权成像(diffusion weighted imaging,DWI)表现及最小表观弥散系数(apparent diffusion coefficient,ADC)值,探讨最小ADC值对其鉴别诊断价值,提高其术前定性诊断的能力。

1 材料与方法

1.1 研究对象

       收集2012年3月至2019年6月我院经手术及病理证实的22例腹膜后pNT患儿资料,其中节细胞神经瘤5例,节神经母细胞瘤7例,神经母细胞瘤10例,男14例女8例,年龄5个月至13岁,中位年龄3岁;位于左侧12例,右侧10例;临床表现为腹部膨隆8例,呕吐5例,呕吐伴发热3例,双下肢疼痛无力4例,无明显阳性体征2例。所有患儿均为初诊,检查前均未接受放化疗及活检手术。

1.2 仪器与方法

       扫描采用PhilipsIngenia 3.0 T MRI扫描仪,16通道体部线圈,运用呼吸门控技术。检查前禁食4~6 h,对不能配合检查的患儿于检查前20~30 min给予10%水合氯醛(50 mg/kg体质量)口服,待其熟睡后行MRI。平扫:T1加权像(T1 weighted imaging,T1WI)快速梯度回波(turbo field echo ,TFE)重复时间(repetition time ,TR) 10 ms,回波时间(echo time ,TE) 2.3 ms,视野240 mm×240 mm~300 mm×300 mm,矩阵200×121,激励次数2;T2加权像(T2 weighted imaging,T2WI)快速扫描序列(turbo spin echo ,TSE)高分辨扫描,TR 1200 ms ,TE 80 ms,视野240 mm×240 mm~300 mm×300 mm,矩阵232×129;T2WI反转恢复序列(spectral presaturation with inversion recovery ,SPIR)脂肪抑制技术,TR 1000 ms,TE 80 ms,视野240 mm×240 mm~300 mm×300 mm,矩阵232×129;DWI采用平面回波成像(echo planar imaging ,EPI)序列轴位扫描,扫描参数:单层层厚3 mm,层距0.3 mm,视野240 mm×240 mm ,TR 5700 ms ,TE 71 ms,矩阵128×100,同时运用频率选择脂肪抑制技术,扫描范围内上下各加一预饱和带,扩散系数b值为800 s/mm2。增强扫描对比剂采用钆喷酸葡胺(gadopentetate dimeglumine ,Gd-DTPA),剂量0.2 ml/kg体质量,速率2 ml/s,经肘静脉快速推注。注射对比剂后行轴位、矢状位和冠状位T1WI扫描,参数同平扫。

1.3 图像分析

       采用Philips R2.6.3.1工作站进行图像后处理,重建ADC值图,由2~4名放射科主治医师以盲法独立观察图像,如有分歧经协商后达成一致。观察并记录肿瘤位置、数量、大小、形态、信号特点、强化方式及强化程度等。对照增强图像,于重建ADC值图上手动绘制椭圆形感兴趣区(region of interest,ROI),面积均为20~30 mm2,放置于肿瘤强化最明显的实性部分,尽量避开病灶内可见的出血、囊变坏死及钙化区,测量其最小ADC值,测量5次取平均值。

1.4 统计学分析

       采用SPSS (Statistical Product and Service Solutions ) 23.0统计分析软件,计量资料以±s表示,经正态分布检验后,采用独立样本t检验比较三者之间的最小ADC值差异,以病理诊断为金标准,绘制受试者操作特征曲线(receiver operating characteristic curve,ROC)曲线,评价最小ADC值对三者的鉴别诊断效能。P<0.05为差异有统计学意义。

2 结果

2.1 磁共振表现

       5例GN均为单发病灶,T1WI显示4处病灶呈较均匀低信号,1处病灶呈低信号伴边缘稍高信号;T2WI显示1处病灶呈稍高-高信号,另4处病灶呈稍高-高信号伴有内部少许低信号;4例增强扫描病例显示4处病灶均可见不均匀强化,其中2处中重度强化,2处轻度强化。7例GNB均为单发病灶,T1WI显示2处病灶呈稍低-低信号,5处病灶呈稍低-低信号伴有内部少许稍高信号;T2WI显示2处病灶呈稍高-高信号,5处病灶呈稍高-高信号伴有内部少许低信号;4例增强扫描病例显示4处病灶均可见中重度不均匀强化。10例NB均为单发病灶,T1WI显示7处病灶呈等、稍低-低信号,3处病灶呈等-稍低信号伴散在稍高信号;T2WI显示2处病灶呈稍高-高信号,8处病灶呈稍高-高信号伴散在低信号;8例增强扫描病例显示8处病灶中均可见不均匀强化,其中3例轻度强化,其余5例中重度强化。22处病灶DWI均显示高低不一混杂信号(图1图2图3)。

图1  女,8岁,节神经细胞瘤,左侧腹膜后类椭圆形肿块。A:T1WI横断面示病灶呈轻度不均匀等-低信号;B:T2WI横断面示病灶呈混杂稍高-高信号;C:DWI横断面示病灶呈周边稍高信号伴内部稍低信号;D:ADC横断面示病灶呈周边稍低信号,伴内部稍高信号;E:增强扫描示病灶呈中度不均匀强化;F:肿瘤细胞体积大,胞质丰富,肿瘤间质内有较多的黏液基质和胶原纤维束,血管少(HE ×40)
图2  男,3岁,节神经母细胞瘤,右侧腹膜后不规则肿块。A:T1WI横断面示病灶呈轻度不均匀等-低信号;B:T2WI横断面示病灶呈混杂稍高-高信号;C:DWI横断面示病灶呈稍高-高信号;D:ADC横断面示病灶呈稍低-稍高信号;E:增强扫描示病灶呈中-重度不均匀强化;F:呈弥漫片状的瘤细胞浸润,胞体小,胞核深染,胞浆少(HE ×40)
Fig. 1  Female, 8 years old, ganglioneuroma, left retroperitoneal elliptic lump. A: T1WI cross-sectional lesions presented mild non-uniform iso-low signal. B: T2WI cross-sectional lesions presented slightly higher confound-high signal. C: DWI cross-sectional lesions presented peripheral slightly higher signals and internal slightly lower signals. D: ADC cross-sectional lesions presented peripheral slightly lower signal and internal slightly higher signal. E: The enhancement scan presented moderate heterogeneous enhancement. F: Tumor cells are large in size and rich in cytoplasm. There are more mucus matrix and collagen fiber bundles in tumor stroma, and fewer blood vessels (HE ×40).
Fig. 2  Male, 3 years old, ganglioneuroblastomam,right retroperitoneal irregular lump. A: T1WI cross-sectional lesions presented mild non-uniform iso-low signal. B: T2WI cross-sectional lesions presented slightly higher confound-high signal. C: DWI cross-sectional lesions slightly higher-high signal. D: ADC cross-sectional lesions showed slightly lower-slightly higher signal. E: The enhancement scan showed moderate to severe heterogeneous enhancement. F: Diffuse patchy infiltration of tumor cells, small cell body, hyperchromatic nucleus, little cytoplasm (HE ×40).
图3  女,1岁,神经母细胞瘤,右侧腹膜后类椭圆形肿块。A:T1WI横断面示病灶呈轻度不均匀等-低信号;B:T2WI横断面示病灶呈混杂稍高-高信号;C:DWI横断面示病灶呈略混杂高信号;D:ADC横断面示病灶呈略混杂低信号;E:增强扫描示病灶呈轻中度不均匀强化;F:瘤细胞呈小圆形,胞浆少,形成中央为神经原纤维的菊形团(Homer-Wright)结构(HE ×40)
Fig. 3  Female, 1 year old, neuroblastoma,right retroperitoneal elliptic lump. A: T1WI cross-sectional lesions presented mild non-uniform iso-low signal. B: T2WI cross-sectional lesions presented slightly higher confound-high signal. C: DWI cross-sectional lesions showed slightly mixed high signal. D: ADC cross-sectional lesions showed slightly mixed low signal. E: The enhancement scan showed mild to moderate non-uniform enhancement. F: The tumor cells are small round, with little cytoplasm, and form a Homer-Wright structure with neurofibrils in the center (HE ×40).

2.2 3种肿瘤的最小ADC值比较

       三组中神经母细胞瘤的最小ADC值最低,为(0.586±0.146)×10-3 mm2/s,节细胞神经瘤的最小ADC值最高,为(1.160±0.310)×10-3 mm2/s,节神经母细胞瘤的最小ADC值位于两者之间,为(0.794±0.156)×10-3 mm2/s。三组采用独立样本t检验,得到F=15.386,P=0.000077 <0.05。后进一步对任意两组间比较,任意两组之间最小ADC值差异均具有统计学意义,(P=0.003、0.040和0.000017)。

2.3 ROC曲线比较分析

       根据三组的最小ADC值绘制ROC曲线,以最小ADC值=0.706×10-3 mm2/s为临界值时鉴别诊断节细胞神经瘤和节神经母细胞瘤约登指数最大,曲线下面积(area under the curve,AUC)为0.917,鉴别诊断的敏感度为100%,特异度为50%。以最小ADC值=0.665×10-3 mm2/s为临界值时鉴别诊断节神经母细胞瘤和神经母细胞瘤约登指数最大,AUC为0.850,鉴别诊断的敏感度为87.5%,特异度80%,

3 讨论

3.1 常规MRI表现的局限性

       临床常规MRI扫描序列可明确腹膜后肿瘤的位置、大小、累及范围及基本信号变化,是儿童腹部肿瘤首选的检查方法。但儿童腹膜后外周神经母细胞性肿瘤发病年龄无明显特异性,T1WI、T2WI及DWI序列影像学表现存在一定交叉,尤其是对该肿瘤提供准确定性和分级的诊断信息有限,缺乏量化指标,鉴别诊断困难。

3.2 ADC值与pNT病理基础的相关性

       DWI的原理是通过水分子扩散运动的方向和程度来反映组织结构的变化[5]。目前,DWI是唯一能观察活体水分子布朗运动的影像学检查方法,由于其具有无创、快速及敏感等优势[6],多应用于儿童肿瘤的诊断。同时它能检测出与组织含水量有关的早期生理变化指标,因此在临床中对于肿瘤良恶性程度的判断起到重要的作用。但DWI显示信号强度受肿瘤组织的T2信号、扩散敏感梯度(b)等因素影响,而ADC值的大小可以定量反映组织水分子的扩散能力,不同组织测量出的ADC值有所不同[7,8]。因此在实际工作中,一般采用ADC值来定量描述弥散扩张系数对肿瘤内水分子的扩散能力。相关文献认为肿瘤ADC值主要与肿瘤细胞密度、细胞膜完整性等因素相关[9]。ADC值与肿瘤细胞水分子扩散能力呈正相关关系,与DWI信号强度呈负指数关系[10]。Koral等[11]就ADC值与肿瘤细胞密度的相关性进行研究,认为随着肿瘤恶性程度的增加,肿瘤细胞密度会随之增大,从而肿瘤细胞内水分子的弥散受限程度进一步提高,相应ADC值降低。从病理上我们发现GN是由大量施万间质和散在分布的神经元成分构成[12],镜下显示肿瘤细胞体积大,胞质丰富,肿瘤间质内有较多的黏液基质和胶原纤维束,血管少,因此肿瘤细胞内水分子弥散程度无明显受限,ADC值显示高;NB富于细胞性神经母细胞肿瘤,缺乏明显施万间质[12],镜下显示瘤细胞呈小圆形,胞浆极少,形成中央为神经原纤维的菊形团(Homer-Wright)结构,病理特征体现出肿瘤细胞内水分子弥散受限程度明显,ADC值显示低;而GNB显示施万基质中混有神经母细胞巢[12],镜下显示弥漫片状的瘤细胞浸润,胞体较小,胞核深染,胞浆较少,病理形态介于神经母细胞瘤和节神经瘤之间,因此肿瘤细胞内水分子弥散受限程度及ADC值均介于GN和NB二者之间,与文献描述一致。

3.3 ADC值方法的选择

       目前一般有三种测量肿瘤ADC值的方法,分别是瘤体平均ADC值、最小ADC值及相对表观扩散系数(relative apparent diffusion coefficient,rADC)(即肿瘤实性成分与周围正常实性组织的ADC比值)。有文献[13]显示无选择性的测量肿瘤整体病灶平均ADC值时,ROI选择时将无法回避病灶内存在的钙化、囊变及坏死区,容易使ADC值产生偏差,对肿瘤的病理特性表达存在一定的局限。本研究中的22例中有21例进行了CT扫描,显示12例病灶内伴有不同程度的钙化,更易体现出平均ADC值测量的局限性。Pierce等[14]对最小ADC值和rADC值在肿瘤的鉴别诊断能力上进行了比较,认为二者的鉴别价值差别不大,但rADC值测量方法在临床日常工作中的使用步骤比较繁琐,因此测量最小ADC值方法会更加简单、更易临床推广运用,同时有文献显示由于肿瘤的异质性,肿瘤实性区域的最小ADC值可以更好地反映异型性肿瘤细胞的最密集区域[15],可以作为评价肿瘤良恶性程度及病理分级的指标,更为准确地反映肿瘤不同的病理级别差异性[16,17]。本研究采用的最小ADC值诊断阈值鉴别三种肿瘤具有统计学意义。

3.4 本研究的局限性

       新版世界卫生组织(World Health Organization,WHO)参照国际神经母细胞性肿瘤病理分类(International Neuroblastoma Pathology Classification,INPC),将外周神经母细胞性肿瘤分为七个亚型[1],不同亚型之间肿瘤的病理特征有所区别,从而导致肿瘤的最小ADC值有所差异,因此有可能会出现部分肿瘤最小ADC值数据的相互重叠。本研究局限于所收集的病理结果并未对肿瘤亚型进行具体分类,因此未将肿瘤亚型之间的最小ADC值差异考虑进此次研究中。另外,考虑到手术中肿瘤的病理标本选取与影像学中最小ADC值的选取区域存在误差的可能性,从而可能导致最小ADC值的测量与组织病理学的相关性仍会存在差异。

       综上所述,最小ADC值在儿童常见腹膜后pNT的鉴别诊断中具有较高的临床应用价值,可在结合常规MRI平扫和增强的图像后,为临床的进一步治疗及其预后提供更多指导和帮助。

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