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Diagnostic value of 18F-FDG PET/CT in intracranial primary central nervous system lymphoma

  • Henan Provincial Key Medical Laboratory of Molecular Imaging, Department of Nuclear Medicine, the First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, China

  • Objective To investigate the diagnostic value of fluorine-18 fluorodeoxyglucose (18F-FDG) PET/CT visual and semi-quantitative analyses in intracranial primary central nervous system lymphoma (PCNSL). Methods PET/CT images of 45 patients with PCNSL who underwent 18F-FDG PET/CT examination in the Department of Nuclear Medicine of the First Affiliated Hospital of Zhengzhou University from May 2011 to December 2018 (26 males and 19 females, 57.49±2.54 years old) were retrospectively reviewed and compared with 52 cases of gliomas and 60 cases of brain metastases to evaluate the value of 18F-FDG PET/CT in the diagnosis of intracranial PCNSL. The lesion distribution and morphological characteristics of the 3 groups of patients were visually analyzed, and the maximum standardized uptake value (SUVmax) and the ratio of SUVmax of tumor to white matter (T/WM) were semi-quantitatively analyzed. The mean comparison between the two groups was performed using independent sample t test and adjusted t test. The comparison of the diagnostic efficacy between the two groups and the judgment of the differential diagnosis threshold were performed using receiver operating characteristic (ROC) curve analysis. Results Visually, intracranial PCNSL showed a very high uptake of 18F-FDG in single, focal nodule or mass lesions mostly located in the supratentorial brain. The space-occupying effects of edema, as well as cystic degeneration, were not obvious in PCNSL. Semi-quantitative analysis showed that intracranial PCNSL had the highest SUVmax (gliomas: 9.96±0.48, brain metastases: 11.97±0.58, PCNSL: 26.42±1.17) and T/WM (gliomas: 2.99±0.09, brain metastases: 2.60±0.08, PCNSL: 4.37±0.10) among the three types of tumors with statistical differences (t=13.02 and 11.07, t=10.13 and 13.88, all P=0.000). In the differential diagnosis of intracranial PCNSL and glioma, the area under the ROC curve (AUC) analysis reached the largest value at the SUVmax of 15.8. The AUC for PCNSL and metastatic tumor peaked at the SUVmax of 16.8. The T/WMs of 3.395 and 3.220 were considered the optimal thresholds for the differential diagnosis of intracranial PCNSL from gliomas and brain metastases, respectively. Conclusion 18F-FDG PET/CT imaging can effectively complement the traditional diagnosis of intracranial PCNSL, especially in the differential diagnosis of PCNSL from gliomas and brain metastases.
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    [4] Suh CH, Kim HS, Park JE, et al. Primary Central Nervous System Lymphoma: Diagnostic Yield of Whole-Body CT and FDG PET/CT for Initial Systemic Imaging[J]. Radiology, 2019, 292(2): 440−446. DOI: 10.1148/radiol.2019190133.
    [5] 吴慧. 原发性中枢神经系统淋巴瘤磁共振成像特征[J]. 影像研究与医学应用, 2019, 3(6): 80−81. DOI: 10.3969/j.issn.2096−3807.2019.06.049.Wu H. Magnetic resonance imaging features of primary central nervous system lymphoma[J]. J Imaging Res Med Appl, 2019, 3(6): 80−81. DOI: 10.3969/j.issn.2096−3807.2019.06.049.
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    [9] 杨柳. 18F-FDG PET/CT在原发性中枢神经系统淋巴瘤诊断中的应用价值[D]. 郑州: 郑州大学, 2019.Yang L. The value of 18F-FDG PET/CT in the diagnosis of central nervous system lymphoma[D]. Zhengzhou: Zhengzhou University, 2019.
    [10] 白人驹, 张雪林. 医学影像诊断学[M]. 3版. 北京: 人民卫生出版社, 2001: 36−42.Bai RJ, Zhang XL. Medical imaging diagnostics[M]. 3rd ed. Beijing: People's Medical Publishing House, 2001: 36−42.
    [11] 张晶晶, 刘保平, 阮翘, 等. 椎管内原发性弥漫性大B细胞淋巴瘤<sup>18</sup>F-FDG PET/CT显像一例[J]. 中华核医学与分子影像杂志, 2018, 38(5): 355−356. DOI: 10.3760/cma.j.issn.2095−2848.2018.05.012.Zhang JJ, Liu BP, Ruan Q, et al. <sup>18</sup>F-FDG PET/CT imaging in intra-spinal canal primary diffuse large B cell lymphoma: a case report[J]. Chin J Nucl Med Mol Imaging, 2018, 38(5): 355−356. DOI: 10.3760/cma.j.issn.2095−2848.2018.05.012.
    [12] 崔向丽, 贾文清, 初君盛, 等. NCCN2009颅内原发淋巴瘤诊疗指南(译文)[J]. 中国神经肿瘤杂志, 2009, 7(4): 311−314. DOI: CNKI:SUN:CJNO.0.2009−04−018.Cui XL, Jia WQ, Chu JS, et al. NCCN2009 Guidelines for Diagnosis and Treatment of Intracranial Primary Lymphoma (Translation)[J]. Chin J Neuro-Oncol, 2009, 7(4): 311−314. DOI: CNKI:SUN:CJNO.0.2009−04−018.
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Diagnostic value of 18F-FDG PET/CT in intracranial primary central nervous system lymphoma

    Corresponding author: Ruihua Wang, fccwangrh@zzu.edu.cn; 
  • Henan Provincial Key Medical Laboratory of Molecular Imaging, Department of Nuclear Medicine, the First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, China
  • Received Date: 2019-10-29
  • Available Online: 2020-06-25

Abstract:  Objective To investigate the diagnostic value of fluorine-18 fluorodeoxyglucose (18F-FDG) PET/CT visual and semi-quantitative analyses in intracranial primary central nervous system lymphoma (PCNSL). Methods PET/CT images of 45 patients with PCNSL who underwent 18F-FDG PET/CT examination in the Department of Nuclear Medicine of the First Affiliated Hospital of Zhengzhou University from May 2011 to December 2018 (26 males and 19 females, 57.49±2.54 years old) were retrospectively reviewed and compared with 52 cases of gliomas and 60 cases of brain metastases to evaluate the value of 18F-FDG PET/CT in the diagnosis of intracranial PCNSL. The lesion distribution and morphological characteristics of the 3 groups of patients were visually analyzed, and the maximum standardized uptake value (SUVmax) and the ratio of SUVmax of tumor to white matter (T/WM) were semi-quantitatively analyzed. The mean comparison between the two groups was performed using independent sample t test and adjusted t test. The comparison of the diagnostic efficacy between the two groups and the judgment of the differential diagnosis threshold were performed using receiver operating characteristic (ROC) curve analysis. Results Visually, intracranial PCNSL showed a very high uptake of 18F-FDG in single, focal nodule or mass lesions mostly located in the supratentorial brain. The space-occupying effects of edema, as well as cystic degeneration, were not obvious in PCNSL. Semi-quantitative analysis showed that intracranial PCNSL had the highest SUVmax (gliomas: 9.96±0.48, brain metastases: 11.97±0.58, PCNSL: 26.42±1.17) and T/WM (gliomas: 2.99±0.09, brain metastases: 2.60±0.08, PCNSL: 4.37±0.10) among the three types of tumors with statistical differences (t=13.02 and 11.07, t=10.13 and 13.88, all P=0.000). In the differential diagnosis of intracranial PCNSL and glioma, the area under the ROC curve (AUC) analysis reached the largest value at the SUVmax of 15.8. The AUC for PCNSL and metastatic tumor peaked at the SUVmax of 16.8. The T/WMs of 3.395 and 3.220 were considered the optimal thresholds for the differential diagnosis of intracranial PCNSL from gliomas and brain metastases, respectively. Conclusion 18F-FDG PET/CT imaging can effectively complement the traditional diagnosis of intracranial PCNSL, especially in the differential diagnosis of PCNSL from gliomas and brain metastases.

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  • 颅内原发性中枢神经系统淋巴瘤（primary central nervous system lymphoma，PCNSL）是一种罕见的中枢神经系统恶性肿瘤，属于侵袭性结外非霍奇金淋巴瘤，病理类型多为弥漫性大B细胞淋巴瘤[1]。虽然其发病率低，但恶性程度很高[2-3]。目前，颅内PCNSL的初步诊断依赖CT、MRI，但因颅内PCNSL与颅内其他常见占位性疾病（如胶质瘤、恶性肿瘤的颅内转移病灶）在CT、MRI的影像学表现上存在诸多相似之处[4-6]，因此误诊率仍然较高。18F-FDG PET/CT显像是融合解剖与功能信息的影像学模式，综合解剖结构信息和葡萄糖代谢状态来分析病灶特点[7-8]。我们回顾性分析经病理学结果证实的颅内PCNSL患者的18F-FDG PET/CT影像资料，总结影像学特征，并分析颅内PCNSL与脑胶质瘤和脑转移瘤的18F-FDG PET/CT影像的鉴别诊断阈值，以提高对该病的认识。

1.   资料与方法

    1.1.   一般资料

  • 收集2011年5月至2018年12月于郑州大学第一附属医院核医学科行18F-FDG PET/CT检查的颅内PCNSL患者45例，年龄（57.49±2.54）岁。其中，男性26例，年龄14~80（58.5±3.4）岁；女性19例，年龄14~77（56.1±3.8）岁。将同期行18F-FDG PET/CT检查的52例脑胶质瘤患者[男性27例，年龄38~75（57.0±2.1）岁；女性25例，年龄33~79（55.2±3.3）岁]和60例脑转移瘤患者[男性31例，年龄40~74（58.5±1.6）岁；女性29例，年龄42~79（60.1±2.1）岁]作为对照组，3组患者之间年龄的差异无统计学意义（男：F=0.11，P=0.892；女：F=1.08，P=0.346）。患者纳入标准：（1）均在18F-FDG PET/CT检查后经病理学确诊；（2）检查前未曾行激素治疗或任何放疗、化疗。排除标准：（1）存在人类疱疹病毒4感染症状及证据；（2）存在免疫功能缺陷病史（包括先天性或获得性）。行18F-FDG PET/CT检查前所有患者或其家属均签署了知情同意书。

    • 1.2.   检查方法及诊断标准

  • 患者空腹6~8 h，经肘静脉注射18F-FDG（由日本住友集团医用回旋加速器自动化合成模块合成），注射剂量按照3.70~5.55 MBq/kg体重计算。患者取仰卧位，采用德国Siemens公司的Biograph Truepoint 64 PET/CT仪进行扫描。CT扫描参数：管电压120 kV，管电流120~250 mAs，层厚3 mm。PET采用三维扫描模式，头部扫描3 min/床位，体部扫描1.5 min/床位，扫描范围从颅顶至股骨上段。CT衰减校正后进行迭代法重建。

    18F-FDG PET/CT图像由2名有3年以上独立诊断经验的医师进行视觉分析，意见不一致时咨询上级医师。18F-FDG代谢情况以周围正常脑白质或对侧相应部位脑白质18F-FDG摄取水平为标准[9]：病灶代谢活跃程度高记为阳性，活跃程度低记为阴性。病灶形态判断及描述以颅脑CT诊断为标准[10]。PET/CT半定量分析基于SUVmax、肿瘤与对侧相应部位脑组织SUVmax的比值（the ratio of SUVmax of tumor to white matter，T/WM），勾画ROI，应用计算机ROI技术和Syngo工作站（德国Siemens公司）进行计算。

    • 1.3.   统计学分析

  • 采用SPSS17.0软件进行统计学分析。符合正态分布的计量资料采用均数±标准差（$\bar x \pm s$）表示。2组间半定量结果的比较采用独立样本t检验（方差齐）和校正后t检验（方差不齐）；2组间诊断效能的比较及鉴别诊断阈值的判断采用ROC曲线分析。P<0.05为差异有统计学意义。

2.   结果

    2.1.   病灶分布特征

  • 45例颅内PCNSL患者经病理学结果证实均为弥漫性大B细胞淋巴瘤，病灶数共70个，多位于脑组织较深的部位，近中线分布多见于脑室周围，体部未见病灶。45例患者中，单发病灶较常见（34/45，75.6%）；70个病灶中，病灶位于幕上者多见（61/70，87.1%）、位于幕下者仅9个（9/70，12.9%）。52例脑胶质瘤患者的病灶数共98个，其中，位于幕上者32个（32/98，32.7%）、位于幕下者66个（66/98，67.3%），经病理学结果证实均为高级别脑胶质瘤。60例脑转移瘤患者的病灶数共129个，其中，位于幕上者15个（15/129，11.6%）、位于幕下者114个（114/129，88.4%），经病理学结果证实原发肿瘤均为肺癌（表1）。

    组别例数单发病灶分布情况多发病灶分布情况
    PCNSL 45 幕上（额叶、顶叶、颞叶、枕叶、基底节区、脑室旁、胼胝体、丘脑）；幕下（小脑） 幕上（额叶、颞叶、顶叶、枕叶、基底节区、侧脑室后角及内侧）；幕下（小脑蚓部、中脑、脑桥）
    脑胶质瘤 52 幕上（额叶、颞叶、顶叶、枕叶、基底节区）；幕下（小脑、中脑、脑干） 幕上（额叶、颞叶、枕叶、基底节区、脑室）；幕下（小脑、脑桥）
    脑转移瘤 60 幕上（额叶、颞叶、顶叶、枕叶）；幕下（小脑、脑干） 幕上（额叶、颞叶、顶叶、枕叶、基底节区、侧脑室）；幕下（小脑、脑桥）
    注：表中，PCNSL：原发性中枢神经系统淋巴瘤

    Table 1.  Distribution characteristics of lesions in the three groups

    • 2.2.   病灶形态特征

  • 颅内PCNSL的实质区呈结节状和团块状，CT表现为等或稍高密度，密度均匀，占位效应不明显，病灶周边水肿区不明显，病灶内继发征象囊变、坏死少见，中线移位、脑室受压较少见，肿瘤实质区对18F-FDG的摄取明显增高（图1）。脑胶质瘤的实质区病灶形态不规则，CT表现为稍低或等密度，占位效应较明显，病灶周边水肿区较明显，肿瘤实质病灶内伴继发征象囊变、出血，个别见钙化，中线移位及脑室受压可见，病灶边缘对18F-FDG的摄取增高，内部囊变、坏死，出血区的摄取减低。脑转移瘤的实质区病灶呈结节状，CT表现为稍低密度或混杂密度，几乎所有的病灶周边均可见中重度水肿，中线移位及脑室受压多见，肿瘤实质病灶边缘对18F-FDG的摄取呈不同程度增高（表2）。

    Figure 1.  18F-FDG PET/CT image of intracranial primary central nervous system lymphoma patient（male，80 years old）

    组别例数密度囊变、坏死水肿中线移位脑室受压18F-FDG摄取程度18F-FDG高摄取的分布情况
    PCNSL 45 等或稍高 少见 轻、重度 少见 少见 显著升高 绝大多数均匀
    脑胶质瘤 52 稍低或等 可见 轻、重度 可见 可见 显著升高 不均匀
    脑转移瘤 60 稍低或混杂 多见 中、重度 多见 多见 不同程度升高 明显不均匀
    注：表中，PCNSL：原发性中枢神经系统淋巴瘤；FDG：氟脱氧葡萄糖

    Table 2.  Morphological characteristics of lesions in the three groups

    • 2.3.   病灶半定量分析结果

  • 对3组患者病灶的半定量分析结果（表3）显示，颅内PCNSL病灶的SUVmax（t=13.02、11.07，均P=0.000）和T/WM（t=10.13、13.88，均P=0.000）明显高于脑胶质瘤和脑转移瘤病灶，且差异有统计学意义。颅内PCNSL的病灶大小和CT值与脑胶质瘤相比，差异无统计学意义（t=0.61、1.40，P=0.546、0.165）；但颅内PCNSL的病灶大小和CT值高于脑转移瘤，差异有统计学意义（t=4.82、2.32，P=0.000、0.023）。

    组别例数病灶大小（cm）CT值（HU）SUVmaxT/WM
    PCNSL 45 3.08±0.12a 37.59±0.83a 26.42±1.17ab 4.37±0.10ab
    脑胶质瘤 52 2.98±0.11 36.02±0.76 9.96±0.48 2.99±0.09
    脑转移瘤 60 2.34±0.09 35.57±0.43 11.97±0.58 2.60±0.08
    注：表中，a：与脑转移瘤相比，差异均有统计学意义（t=2.32~13.88，均P<0.05）；b：与脑胶质瘤相比，差异均有统计学意义（t=13.02、10.13，均P=0.000）。FDG：氟脱氧葡萄糖；PET：正电子发射断层显像术；CT：计算机体层摄影术；PCNSL：原发性中枢神经系统淋巴瘤；SUVmax：最大标准化摄取值；T/WM：肿瘤与对侧相应部位脑组织SUVmax的比值

    Table 3.  Results of the semi-quantitative analysis of lesions in the three groups ($\bar x \pm s $)

    • 2.4.   ROC曲线分析结果

  • ROC曲线分析结果显示，当SUVmax=15.8时，颅内PCNSL与脑胶质瘤鉴别诊断的AUC最大（0.982），灵敏度为95.6%，特异度为94.2%（图2中A）；而当SUVmax=16.8时，颅内PCNSL与脑转移瘤鉴别诊断的AUC最大（0.946），灵敏度为93.3%，特异度为85.0%（图2中B）。当T/WM=3.395时，颅内PCNSL与脑胶质瘤鉴别诊断的AUC最大（0.918），灵敏度为86.7%，特异度为73.1%（图2中C）；而当T/WM＝3.220时，颅内PCNSL与脑转移瘤鉴别诊断的AUC最大（0.973），灵敏度为97.8%，特异度为83.3%（图2中D）。可以认为T/WM=3.395为颅内PCNSL与脑胶质瘤鉴别诊断的最佳阈值，而T/WM=3.220为颅内PCNSL与脑转移瘤鉴别诊断的最佳阈值。

    Figure 2.  The ratio of SUVmax of tumor to white matter (T/WM) and SUVmax ROC curves of primary central nervous system lymphoma (PCNSL), gliomas, and brain metastases

3.   讨论

  • PCNSL较罕见，属结外淋巴瘤，累及全身各个部位的神经轴索，包括颅内、椎管[11]、视神经等，极少累及全身。2009年美国国立综合癌症网络颅内原发淋巴瘤诊疗指南指出，PCNSL患者可以考虑做全身PET扫描，并可替代CT和骨髓检查，但是目前PCNSL患者使用PET诊断的数据仍比较缺乏，18F-FDG PET/CT诊断的数据更是不足[12]。本研究中我们采用18F-FDG PET/CT显像，不仅从影像表现上得到了颅内PCNSL的结构特征，而且通过ROC曲线分析得到了颅内PCNSL与脑胶质瘤和脑转移瘤鉴别诊断的最佳阈值，分享了18F-FDG PET/CT显像在颅内PCNSL诊断中的应用经验。

    本研究结果显示，PCNSL病灶主要集中在中线附近深部脑组织，以单发、结节状、团块状病灶居多，继发改变较少出现，这与文献报道结果类似[5, 13]。PCNSL细胞的生长方式决定了病灶均呈浸润性“蟹足样”生长。密集的、单克隆增殖的淋巴细胞组成的血管聚集型肿瘤细胞突破血脑屏障呈浸润性生长，累及脑实质，“钻缝样”侵入脑组织，早期对脑沟、脑回的形态改变不大，肿瘤病灶周边水肿和内部继发改变不明显。PCNSL与脑胶质瘤和脑转移瘤相比，肿瘤细胞密集、增殖活性强、细胞转运蛋白对18F-FDG的摄取较高，因此有较高的葡萄糖代谢水平[4, 14-16]，但文献报道并未见有公认的SUVmax测量值用于鉴别诊断，这可能与SUVmax的测量值在一定程度上受到的影响因素较多有关，也可能与不同扫描仪器间SUVmax的测量值存在不同程度的差异有关。理论上，T/WM不仅能从数值上反映肿瘤的代谢水平，而且能为不同的扫描仪器和不同的医疗单位的疾病诊断提供借鉴。本研究以T/WM为数据分析点，对18F-FDG PET/CT显像鉴别颅内PCNSL与脑胶质瘤和脑转移瘤作ROC曲线，分析18F-FDG PET/CT显像对颅内PCNSL的诊断价值，预测T/WM=3.395为颅内PCNSL与脑胶质瘤鉴别诊断的临界值，对于T/WM>3.395的患者而言，诊断为PCNSL的可能性更大。而T/WM=3.220可认为是颅内PCNSL与脑转移瘤鉴别诊断的临界值，对于T/WM>3.220的患者而言，诊断为PCNSL的可能性更大。18F-FDG PET/CT显像在PCNSL与脑胶质瘤和脑转移瘤的鉴别诊断上有重要的应用价值。PCNSL在发生部位、形态、代谢的影像表现上与脑胶质瘤和脑转移瘤有相似之处，半定量分析指标上与脑胶质瘤、脑转移瘤也有交叉重合。通常来说，PCNSL易发于深部脑组织，脑胶质瘤可发生于任何部位，脑转移瘤则多发生在皮髓质交界处；PCNSL以单发最常见，脑胶质瘤的单发病灶稍多于多发病灶，脑转移瘤则以多发病灶常见；PCNSL、脑胶质瘤早期不改变脑沟、脑回形态，脑转移瘤改变脑沟、脑回形态较早；PCNSL病灶周边水肿不明显，脑胶质瘤病灶周边水肿比PCNSL重，而脑转移瘤则常出现“小病灶，大水肿”；PCNSL病灶中继发改变少见，脑胶质瘤继发改变比PCNSL明显，而脑转移瘤的继发改变最常见；PCNSL、脑胶质瘤病灶较大，脑转移瘤较小；PCNSL、脑胶质瘤实质病灶的CT值较高，脑转移瘤较低；PCNSL的SUVmax较大，脑胶质瘤、脑转移瘤较小；PCNSL的T/WM最大，脑胶质瘤次之，脑转移瘤最小。PCNSL与脑胶质瘤和脑转移瘤的鉴别诊断需要根据以上特征进行综合分析，而18F-FDG PET/CT显像可在一次检查中提供以上所有信息。

    本研究中我们以视觉分析和半定量分析探讨18F-FDG PET/CT显像在PCNSL中的应用价值，但仍有不足之处。我们仅用了CT平扫进行诊断，没有发挥增强CT的诊断价值，以后将使用增强CT扫描，为PCNSL的诊断和鉴别诊断提供更多的信息。本研究结果显示，颅内PCNSL对18F-FDG的摄取程度远高于颅内对侧脑皮质，在没有条件生产11C-甲基-L-蛋氨酸等颅内低本底显像剂的单位，用常规显像剂18F-FDG即可满足对PCNSL的诊断，但由于颅内灰质和基底核团对18F-FDG的摄取较高，导致高摄取背景影响对目的病灶的观察，尤其是在低级别胶质瘤和较小颅内转移瘤中，高摄取背景极易掩盖对病灶的观察，如果能够选取其他颅内低摄取的显像剂，如11C-蛋氨酸，则能更好地提高诊断效能，尤其是多种显像剂同时应用时具有巨大的优越性，是未来PET/CT的发展方向，也是PCNSL诊断研究进一步深入的方向。另外，本研究结果显示，3种肿瘤T/WM有一定程度的重合，总体来看PCNSL最高，但是从本研究目前的结果来看，并不能单纯用T/WM来武断地鉴别PCNSL与脑胶质瘤和脑转移瘤，需要依据18F-FDG PET/CT得到的其他参数同时分析判断。SUVmax和T/WM是18F-FDG PET/CT的重要参数，本研究虽然样本量不够大，但也得出了一定的规律，总结了18F-FDG PET/CT SUVmax和T/WM在PCNSL与脑胶质瘤和脑转移瘤鉴别诊断中的应用价值，但由于PCNSL罕见，多中心合作是共同努力的方向，期待更多的研究者加入，继续扩大样本量，使诊断阈值更趋合理化、更具实践性。

    综上，在单纯CT、MRI诊断困难时，18F-FDG PET/CT显像不仅能从形态学上鉴别PCSNL与脑胶质瘤和脑转移瘤，还可以通过葡萄糖代谢的半定量分析结果对其进行进一步有效地鉴别诊断，作为传统影像学诊断的有效补充。虽然18F-FDG PET/CT显像的价格较高，但从早期有效诊断、改善患者预后的角度考虑，且一次检查可以提供多种信息，18F-FDG PET/CT显像仍不失为一种有价值的诊断方法。

    利益冲突　本研究由署名作者按以下贡献声明独立开展，不涉及任何利益冲突。

    作者贡献声明　王瑞华负责研究命题的提出、论文的撰写、最终版本的修订；吴彬彬负责研究命题的设计、数据的获取与分析、最终版本的修订；杨柳负责研究命题的设计、数据的获取与分析；周倩负责数据的获取；张晶晶、刘艳、韩星敏负责论文的审阅及指导。

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