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临床研究
磁共振扩散加权成像ADC值对普通型骨肉瘤新辅助化疗早期疗效的评估价值
李玉增 麦尔哈巴·努尔麦麦提 徐慧 张石峰

Cite this article as: Li YZ, Maierhaba·NEMMT, Xu H, et al. Evaluation of magnetic resonance DWI-ADC value in assessing the early efficacy of neoadjuvant chemotherapy for conventional osteosarcoma[J]. Chin J Magn Reson Imaging, 2022, 13(11): 88-92, 136.本文引用格式:李玉增, 麦尔哈巴·努尔麦麦提, 徐慧, 等. 磁共振扩散加权成像ADC值对普通型骨肉瘤新辅助化疗早期疗效的评估价值[J]. 磁共振成像, 2022, 13(11): 88-92, 136. DOI:10.12015/issn.1674-8034.2022.11.016.


[摘要] 目的 探讨磁共振扩散加权成像(diffusion-weighted imaging, DWI)不同表观扩散系数(apparent diffusion coefficient, ADC)值及其变化率对骨肉瘤新辅助化疗(neoadjuvant chemotherapy, NAC)早期疗效的评估价值。材料与方法 回顾性分析2019年1月至2022年3月期间在新疆医科大学附属肿瘤医院行NAC的骨肉瘤患者病例23例,在NAC前、化疗4周期后进行常规MRI和DWI检查,分别获得不同ADC值及其变化率等参数值。根据病理组织学Huvos分级法将患者按照化疗疗效分为组织学反应良好组与组织学反应差组,比较两组间的不同ADC值[平均ADC值(ADCmean)、最小ADC值(ADCmin)、单位体积的平均ADC值(ADCmean/V)、单位体积的最小ADC值(ADCmin/V)]及其变化率的差异。结果 组织学反应良好组化疗前后ADCmean、ADCmin、ADCmean/V、ADCmin/V差异均有统计学意义,P值均<0.05(分别为0.024、<0.001、0.018、0.046)。组织学反应差组化疗前后ADCmean、ADCmin、ADCmin/V差异均有统计学意义,P值均<0.05(分别为0.005、<0.001、0.020),ADCmean/V差异无统计学意义(P=0.071,P>0.05)。两组间ADCmean、ADCmin、ADCmean/V、ADCmin/V的变化率差异均有统计学意义,P值均<0.05(分别为0.047、0.006、0.039、0.015)。经受试者工作特征(receiver operating characteristic, ROC)曲线分析ADCmin变化率曲线下面积(area under the curve, AUC)为0.938,高于ADCmean、ADCmin/V、ADCmean/V等变化率(AUC分别为0.783、0.767、0.813)。结论 不同ADC值及其变化率对骨肉瘤早期疗效评估具有重要价值,ADCmin变化率在骨肉瘤疗效预测中具有显著优势。
[Abstract] Objective To investigate the value of different apparent diffusion coefficient (ADC) value of magnetic resonance diffusion-weighted imaging (DWI) and their rates of change in assessing the early efficacy of neoadjuvant chemotherapy for osteosarcoma.Materials and Methods Cases of twenty-three patients with osteosarcoma undergoing neoadjuvant chemotherapy (NAC) at the Affiliated Tumour Hospital of Xinjiang Medical University between January 2019 and March 2022 were collected, and conventional MRI and DWI were performed before NAC and after 4 cycles of chemotherapy to obtain different ADC value and its rate of change were obtained. Patients were divided into good histological response group and poor histological response group according to the pathological histological Huvos grading method of chemotherapy, and the statistical differences of different ADC value and their change rates between the two groups were compared.Results The differences in ADCmean, ADCmin, ADCmean/volume, ADCmin/volume before and after chemotherapy in the good histological response group were statistically significant, all P<0.05 (P values were 0.024, <0.001, 0.018, 0.046, respectively). The differences in ADCmean, ADCmin, ADCmin/volume before and after chemotherapy were statistically significant in the poor histological response group, all P<0.05 (P values were 0.005, <0.001, 0.020, respectively), while the differences in ADCmean/volume were not statistically significant (P=0.071, P>0.05). The differences in the rates of change of ADCmean, ADCmin, ADCmean/volume, and ADCmin/volume between the two groups were statistically significant (P=0.047, 0.006, 0.039, 0.015, all P<0.05). The area under the curve (AUC) of ADCmin rate of change by receiver operating characteristic (ROC) curve analysis was 0.938, which was higher than the rates of change of ADCmean, ADCmin/volume, and ADCmean/volume (0.783, 0.767, and 0.813, respectively).Conclusions Different ADC value and their rates of change are of great value in the early assessment of the efficacy of osteosarcoma, and the ADCmin rate of change has significant advantages in predicting the efficacy of osteosarcoma.
[关键词] 骨肉瘤;新辅助化疗;疗效评估;曲线下面积;表观扩散系数;扩散加权成像;磁共振成像
[Keywords] osteosarcoma;efficacy evaluation;neoadjuvant chemotherapy;area under the curve;apparent diffusion coefficient;diffusion weighted imaging;magnetic resonance imaging

李玉增    麦尔哈巴·努尔麦麦提    徐慧 *   张石峰   

新疆医科大学附属肿瘤医院影像中心,乌鲁木齐 830011

徐慧,E-mail:simplehui2004@163.com

作者利益冲突声明:全体作者均声明无利益冲突。


收稿日期:2022-07-08
接受日期:2022-10-15
中图分类号:R445.2  R738.1 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.11.016
本文引用格式:李玉增, 麦尔哈巴·努尔麦麦提, 徐慧, 等. 磁共振扩散加权成像ADC值对普通型骨肉瘤新辅助化疗早期疗效的评估价值[J]. 磁共振成像, 2022, 13(11): 88-92, 136. DOI:10.12015/issn.1674-8034.2022.11.016

       骨肉瘤是最常见的骨原发性恶性肿瘤,占骨原发恶性肿瘤的20%[1]。好发于儿童和青少年,特别是12~18岁儿童和青少年,已成为该年龄段仅次于白血病和淋巴瘤的最常见的第三大癌症类型,严重威胁着青少年的身心健康[2, 3]。骨肉瘤来源于间叶组织,能产生骨样组织和非成熟骨组织,致死致残率极高[4]。20世纪70年代,随着新辅助化疗(neoadjuvant chemotherapy, NAC)技术的兴起及应用,患者的五年生存率由20%上升到70%,大大延长了患者生存时间[5, 6]。功能MRI可以通过肿瘤内部水分子的运动、血流灌注及毛细血管的通透性等情况来评估化疗疗效[7]。扩散加权成像(diffusion-weighted imaging, DWI)是唯一能够反映活体组织水分子的扩散程度和细胞内、外水分子的转运情况的成像方法,而表观扩散系数(apparent diffusion coefficient, ADC)可定量分析不同组织水分子扩散的速度以及扩散受限的程度,从而在分子水平对病变进行评估[8],目前广泛应用于乳腺癌、肝癌、直肠癌、宫颈癌等疾病的预后评估[9, 10, 11, 12]。ADC值在骨肉瘤疗效评估中的应用也有研究,但却缺乏进一步对平均ADC值(ADCmean)、最小ADC值(ADCmin)在疗效评估中价值的研究。而本研究通过比较两组骨肉瘤患者化疗前后ADCmean、ADCmin及其变化率等参数值的差异,来探讨不同参数值对骨肉瘤NAC早期疗效的评估效能。同时本研究在国内也首次引用单位体积的ADC(ADC值/体积)这一新的评估参数,并进一步将ADCmean/体积(ADCmean/V)、ADCmin/体积(ADCmin/V)参数值应用于骨肉瘤疗效评估。

1 材料与方法

1.1 临床资料

       本研究遵守《赫尔辛基宣言》,并经新疆医科大学附属肿瘤医院伦理委员会批准,免除受试者知情同意,批准文号:K-2022018。本研究回顾性分析2019年1月至2022年3月期间新疆医科大学附属肿瘤医院治疗的普通型骨肉瘤患者病例23例,男15例,女8例,年龄7~30(15.4±5.8)岁。纳入标准:(1)NAC前经病理穿刺结果确诊为骨肉瘤患者;(2)在我院进行系统NAC治疗,病历资料完整;(3)化疗前一周内、四周期化疗后一周内分别行MRI检查(包括平扫、增强和DWI扫描);(4)手术切除完整病变,且术后具有明确的病理组织学结果。排除标准:(1)入院前进行相关的药物或者手术干预患者;(2)心力衰竭、肝肾功能衰竭等严重系统性疾病;(3)MRI图像不佳,影响病变诊断及后处理。

1.2 MRI扫描

       采用飞利浦3.0 T MR设备(Ingenia 3.0 T, Philips Healthcare, Netherlands);根据病变范围于NAC前一周内、四周期化疗后一周内选用膝关节线圈或体线圈进行扫描。平扫序列及参数:扫描冠状位及轴位快速自旋回波(turbo spin echo, TSE)T1WI序列(TR 500 ms,TE 15 ms)、冠状位及轴位SPAIR脂肪抑制T2WI序列(TR 2000 ms,TE 45 ms)、轴位TSE T2WI序列(TR 3000 ms,TE 75 ms);FOV均为320 mm×400 mm;层厚均为5 mm,层间距均为1 mm。DWI序列参数:TR 6000 ms,TE 70 ms,FOV 400 mm×300 mm,层厚5 mm,层间距1 mm,扩散敏感系数b值取0、1000 s/mm2,同时在X轴、Y轴、Z轴施加扩散敏感梯度场。增强序列及参数:扫描轴位及冠状位脂肪抑制T1WI,TR 816 ms,TE 8 ms,FOV 300 mm×400 mm,层厚5 mm,层间距1 mm,对比剂使用马根维显(Magnevist, Berlin, Germany),由肘静脉手推注入,剂量0.2 mL/kg。

1.3 MRI图像处理

       由2名具有5年以上影像学诊断经验的医师利用飞利浦星云搜索平台(IntelliSpace Discovery, ISD)进行图像病灶感兴趣区(region of interest, ROI)勾画。肿瘤体积的获取:在增强扫描横轴位脂肪抑制T1WI图像对实质区域ROI进行3D勾画,获取病灶体积。结合T2WI和DWI图像,确定ADC图像上的病灶范围。以b=1000 s/mm2作为ADC的b值,在病灶实质区域放置ROI,注意避开出血、囊变、坏死及钙化区域,每个病灶进行三次测量并获取ADCmean、ADCmin,取测量结果的平均值,并计算其与病灶体积的比值及变化率。计算ADC值变化率=(ADC值化疗后-ADC值化疗前)/ADC值化疗前×100%。

1.4 病理组织学判定

       由2位副主任以上职称的病理科专家共同观察骨肉瘤切除术后病理标本进行诊断工作,若意见一致则为最后诊断结果,如不一致则进行全科讨论,计算得出每个病灶的肿瘤坏死率。NAC疗效判定的金标准参照病理组织学Huvos分级法[13],肿瘤坏死率≥90%为组织学反应良好组(包括Huvos Ⅲ和Ⅳ级),肿瘤坏死率<90%为组织学反应差组(包括Huvos Ⅰ和Ⅱ级)。

1.5 统计学分析

       采用SPSS 26.0统计学软件对相关数据进行分析。计量资料符合正态分布时采用均数±标准差(x¯±s)表示。组间比较数据符合正态性、方差齐性时采用独立样本检验;组内比较采用配对检验。术后病理组织学分级作为判断NAC疗效的金标准,探讨ADCmean、ADCmin、ADCmean/V、ADCmin/V及其变化率等对化疗疗效的预测价值。以Spearman等级相关分析不同ADC变化率与化疗疗效的相关性。P<0.05为差异具有统计学意义。

2 结果

       对23例普通型骨肉瘤患者行4周期NAC后进行手术,术后病理结果显示组织学反应良好组8例,组织学反应差组15例。

2.1 组内不同ADC比较

       组织学反应良好组及反应差组化疗前后ADCmean、ADCmin、ADCmin/V差异均有统计学意义(P<0.05)。反应良好组ADCmean/V化疗前后差异有统计学意义(P=0.018),反应差组ADCmean/V化疗前后差异无统计学意义(P=0.071)(表1图1)。

图1  女,23岁,左侧股骨上段普通型骨肉瘤。1A~1D为患者新辅助化疗前的影像与病理资料,该患者病变区域信号不均,扩散加权成像(DWI)序列以高信号为主,病灶扩散受限(1A),轴位T2WI脂肪抑制序列显示病灶以高信号为主(1B),轴位T1WI序列以稍低信号为主(1C),病理图(HE ×200)为病变穿刺结果,显示为普通型骨肉瘤(1D);1E~1H为患者经过4周期新辅助化疗后的影像与病理资料,DWI序列以高信号为主(1E),轴位T2WI脂肪抑制序列以稍高信号为主(1F),轴位T1WI序列呈稍低信号(1G),病理图(IHC ×200)为截肢术后结果,显示为普通型骨肉瘤,病理坏死分级Ⅲ级(1H)。
Fig. 1  Female, 23 years old, conventional osteosarcoma of the left upper femoral segment. 1A-1D show the imaging and pathological data of the patient before neoadjuvant chemotherapy, this patient has an uneven signal in the area of the lesion. Diffusion-weighted image (DWI) is dominate by high signal and limit lesion diffusion (1A). Axial T2-weighted fat suppression sequence is dominate by high signal (1B). Axial T1WI sequence is dominate by slightly low signal (1C). The pathological image (HE ×200) show the puncture results of the lesions, indicating conventional osteosarcoma (1D). 1E-1H show the imaging and pathological data of the patient after 4 cycles of neoadjuvant chemotherapy. DWI is dominate by high signal (1E). Axial T2-weighted fat suppression sequence is dominate by slightly high signal (1F). Axial T1WI sequence shows slightly low signal (1G). The pathological image (IHC ×200) shows the results after amputation, indicating conventional osteosarcoma with grade Ⅲ pathological necrosis.
表1  新辅助化疗前后不同疗效组不同ADC值比较
Tab. 1  Comparison of different apparent diffusion coefficients in different efficacy groups before and after neoadjuvant chemotherapy

2.2 组间不同ADC值及变化率比较

       化疗前两组间ADCmean、ADCmin、ADCmean/V、ADCmin/V差异均没有统计学意义,P值均>0.05(分别为0.502、0.135、0.533、0.933)。

       反应良好组体积为(-163.12±189.30)cm3,反应差组体积为(96.52±498.62)cm3,差异无统计学意义(P=0.174)。两组间ADCmean、ADCmin、ADCmean/V、ADCmin/V的变化率差异均有统计学意义,P值均<0.05(分别为0.047、0.006、0.039、0.015)(表2)。

表2  不同疗效新辅助化疗前后不同ADC变化率比较
Tab. 2  Comparison of the rate of change of different apparent diffusion coefficients before and after neoadjuvant chemotherapy with different efficacy

2.3 不同ADC变化率评估化疗疗效的效能及与化疗疗效相关性

       通过受试者工作特征(receiver operating characteristic, ROC)曲线及曲线下面积(area under the curve, AUC)分析不同ADC值变化率对NAC疗效的评估价值,检验水准为α=0.05。ADCmean、ADCmin、ADCmean/V、ADCmin/V变化率AUC分别为0.783、0.938、0.817、0.767,ADCmin变化率诊断效能高于其他指标,ADCmin变化率的截断值为0.355时,诊断准确度较高(约登指数=0.742),其特异度为87.5%,敏感度为86.7%(表3图2)。

       ADCmin、ADCmean、ADCmean/V、ADCmin/V变化率与化疗疗效均呈负相关性,P均<0.05,相关系数r分别为-0.724、-0.469、-0.523、-0.440。

图2  不同表观扩散系数值变化率受试者工作特征曲线图。
Fig. 2  Receiver operating characteristic curve with different apparent diffusion coefficients value change rates.
表3  不同ADC值变化率疗效评估的效能
Tab. 3  Efficacy assessment of different apparent diffusion coefficients value change rates

3 讨论

       骨肉瘤血供丰富,生长速度快,恶性程度高,致死致残率极高[14],故需要早期有效评估患者的化疗疗效,及时对NAC药物进行调整,争取达到最佳的治疗效果[15]。MRI在反映肿瘤内部病理变化和对神经、周围组织的受侵范围显示上有优势,能够较X线、CT等更早、更准确显示早期病变、髓内受侵、脊髓水肿及跳跃病灶等[16],且有专家认为MRI图像与病理标本对应良好,具有统计学意义[17]。故MRI已成为早期评估肿瘤化疗疗效、预测肿瘤是否复发和能否进行保肢手术的重要方式[18]。目前在骨肉瘤疗效评估中的文献中大多以ADC值研究较多,但却缺乏进一步对ADCmean、ADCmin等评估价值的研究。而本研究通过对ADCmean、ADCmin及其变化率等参数值在骨肉瘤NAC早期疗效的评估中的应用,发现两组间ADCmin与ADCmean变化率差异均有统计学意义;且ADCmin变化率较ADCmean变化率与化疗疗效相关性更为显著,同时对于NAC疗效的诊断效能更高。同时本研究在国内也首次引用ADC值/体积这一新的评估参数,并进一步将ADCmean/V、ADCmin/V及变化率等参数值应用于骨肉瘤疗效评估,发现ADCmean/V、ADCmin/V的变化率同样具有化疗疗效评估价值。

3.1 DWI和ADC在骨肉瘤疗效评估中的应用

       DWI序列的优势在于它是目前唯一可以对活体组织内水分子扩散运动进行无创监测的方法,能够通过水分子扩散的程度反映组织间差异及病理变化[19]。而不同组织水分子扩散的速度以及扩散受限的程度可通过DWI所得到的ADC值进行定量分析,从而在分子水平对组织病理变化进行评估[20]。水分子的扩散运动受到细胞内细胞器、细胞膜以及细胞外空间的影响,DWI序列对水分子扩散程度的反映主要依赖于单位高倍视野的细胞数量[21]。DWI上的信号强度与水分子的自由运动和扩散梯度成反比[22]。经过系统NAC治疗后,肿瘤细胞发生坏死、减少,细胞结构发生破坏,核浆比例减低,水分子扩散程度较前增加,故DWI信号轻度减低,ADC值升高[23, 24, 25]。本研究中,化疗后病变的不同ADC值都出现了不同程度的增高,且组织学反应良好组比化疗前、组织学反应差组增高程度明显。

3.2 ADCmin与ADCmean变化率在骨肉瘤疗效评估中的应用

       本研究还发现化疗反应良好组与反应差组之间ADCmin与ADCmean变化率差异均有统计学意义;且ADCmin变化率较ADCmean变化率对于NAC疗效的评估更有效。分析原因可能是骨肉瘤细胞构成异质性明显,特别是化疗后ADC值变化很大,故ADCmean不一定能够反映肿瘤中较高的细胞密集程度,而细胞密度最高的区域最能反映肿瘤的特征,ADCmin可以反映残余存活肿瘤区域的肿瘤细胞密度,更适合用于骨肉瘤NAC后的疗效评估[26]。马焕等[27]通过对17例骨肉瘤患者分析,同样证实ADCmin变化率较ADCmean变化率是评价骨肉瘤NAC预后更为有效的指标。而王展等[28]通过对78例骨肉瘤患者研究,同样证实反应良好组ADC值变化率大于反应差组,差异有统计学意义。

3.3 ADC值/体积及变化率在骨肉瘤疗效评估中的应用

       Bajpai等[29]提出了ADC值/体积这一新的评估参数,并发现该参数与NAC前、后的组织学反应显著相关。ADC值/体积这一参数的提出,通过描述相对于肿瘤体积的ADC,对化疗疗效评估提供了新的思路。虽然目前该参数用于肿瘤的疗效评估较少,但是本研究发现组织学反应良好组化疗前后ADCmean/V、ADCmin/V差异均有统计学意义。同时本研究还发现反应良好组与反应差组之间ADCmean/V、ADCmin/V的变化率差异有统计学意义。ADCmean/V、ADCmin/V可以用于骨肉瘤化疗疗效的评估,分析原因可能是单位体积的水分子扩散程度及细胞结构改变也能够反映出病灶病理变化程度。

3.4 不同ADC变化率对骨肉瘤疗效的诊断效能及与化疗疗效相关性分析

       本研究通过ROC曲线分析了ADCmean、ADCmin、ADCmean/V、ADCmin/V等变化率对化疗疗效的判定效能,结果发现ADCmean、ADCmean/V、ADCmin/V等变化率AUC在0.7~0.9之间,具有一定诊断效能;ADCmin变化率在判定效能方面高于其他参数,AUC可达到0.938,根据约登指数得到截断值为0.355时,诊断准确度较高,为临床的疗效判定提供了重要参考;同时也发现不同ADC变化率与化疗疗效均呈负相关性,而且ADCmin变化率与化疗疗效相关性较其他参数值更显著,可能是因为ADCmin变化率更能够反映残余病灶区域的肿瘤活性,对病灶化疗疗效评估更敏感。Oka等[26]也指出ADCmin变化率可能是骨肉瘤有用的预后因素。Delli等[30]通过对46例直肠癌患者放化疗8周后的疗效评估发现,ADC值变化率的AUC为0.94,同样证明ADC变化率具有显著的诊断价值。但是本研究发现ADCmean/V与ADCmin/V变化率预测价值相对较低,而且ADCmin/V变化率预测价值低于ADCmean/V变化率,可能是骨肉瘤病变异构性明显,而且涉及化疗前后体积及ADC值等变量较多,另外,b值的选择、ROI勾画及数据测量方法不同,均可导致结果复杂多变。

3.5 局限性与展望

       本研究存在不足之处,首先,本组研究为单中心研究,且样本量相对较少;其次,未对ROI勾画方法、b值等影响因素分别进行分析。在今后的研究中需要加大样本量,并且利用不同勾画方法、b值等加以验证。

       综上所述,本组研究发现:(1)不同ADC值及其变化率对骨肉瘤早期疗效评估均具有重要价值,且ADCmin变化率对骨肉瘤疗效评估效能及相关性显著程度高于其他参数值;(2)ADC值/体积这一新的评估参数为骨肉瘤疗效评估提供了新的方向,且ADCmean/V、ADCmin/V在骨肉瘤疗效评估中均有评估价值。

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