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Comparative analysis of the application value of 18F-FDG PET/MRI and MRI in preoperative T, N staging of patients with esophageal cancer

  • 1.

    Department of Nuclear Medicine, the Second Affiliated Hospital of Air Force Medical University, Xi'an 710024, China

  • 2.

    Department of Nuclear Medicine, Shaanxi Provincial Cancer Hospital, Xi'an 710061, China

  • 3.

    Department of Nuclear Medicine, the Second Affiliated Hospital of Shanxi Medical University, Taiyuan 030001, China

  • Corresponding author: Yunbo Li, 59199548@qq.com ; 
  • Received Date: 2021-02-22
  • Objective To compare the application value of 18F-fluorodeoxyglucose (FDG) PET/MRI and MRI in the preoperative T and N staging of patients with esophageal cancer. Methods The clinical and imaging data of 30 patients who underwent radical resection for esophageal cancer in the Second Affiliated Hospital of the Air Force Military Medical University from January 2018 to December 2019 were retrospectively analyzed. The sample included 25 males and 5 females, aged 42–77(62.9±8.0) years old. All patients underwent 18F-FDG PET/MRI examination within 2 weeks before operation, and the postoperative histopathological examination results were used as the “gold standard” for staging. The Kappa test was employed to evaluate the consistency of 18F-FDGPET/MRI and MRI in the preoperative T and N staging of patients with esophageal cancer and in postoperative histopathological staging. The staging accuracy was compared using the χ2 test, and the values of the maximum standardized uptake (SUVmax), mean standardized uptake (SUVmean), apparent diffusion coefficient minimum vaalue (ADCmin), and apparent diffusion coefficient mean value (ADCmean) of metastatic lymph nodes and benign lymph nodes were compared using independent sample t test. Results 18F-FDG PET/MRI and MRI showed strong consistency in the preoperative T staging and postoperative histopathological staging of patients with esophageal cancer (Kappa value=0.757, 0.698; both P<0.001). The accuracy rates of 18F-FDG PET/MRI and MRI in the diagnosis of preoperative T staging in patients with esophageal cancer were 83.3% (25/30) and 80.0% (24/30) respectively, with no significant difference (χ2=0.110, P>0.05). The diagnostic accuracy of 18F-FDG PET/MRI for preoperative N staging in patients with esophageal cancer was higher than that of MRI (76.7% (23/30) vs. 66.7% (20/30)), and the difference was statistically significant (χ2=11.273, P<0.01). The SUVmax and SUVmean values of the metastatic lymph nodes were higher than those of the benign lymph nodes (5.77±2.66 vs. 2.79±1.29 and 3.16±1.28 vs. 1.78±1.01, respectively), and the difference was statistically significant (t=6.39, 5.96; both P<0.001). Furthermore, the ADCmin of metastatic lymph nodes was lower than that of benign lymph nodes (1.02±0.33 vs. 1.20±0.24), and the difference was statistically significant (t=−3.81, P<0.001). In comparison, there was no statistical significance in the comparison of ADCmean (t=−1.52, P>0.05). Conclusions The value of 18F-FDG PET/MRI in the preoperative T staging of patients with esophageal cancer is comparable to that of MRI, while its diagnostic performance for preoperative N staging of patients with esophageal cancer is better than MRI. Thus, it can be considered the preferred non-invasive preoperative staging method for patients with esophageal cancer.
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  • [1] Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries[J]. CA Cancer J Clin, 2018, 68(6): 394−424. DOI: 10.3322/caac.21492.
    [2] Zhu Y, Fu L, Jing W, et al. The value of magnetic resonance imaging in esophageal carcinoma: tool or toy?[J]. Asia Pac J Clin Oncol, 2019, 15(3): 101−107. DOI: 10.1111/ajco.13112.
    [3] Guo J, Wang ZQ, Qin JJ, et al. A prospective analysis of the diagnostic accuracy of 3T MRI, CT and endoscopic ultrasound for preoperative T staging of potentially resectable esophageal cancer[J]. Cancer Imaging, 2020, 20(1): 64. DOI: 10.1186/s40644-020-00343-w.
    [4] 于军, 张莺, 任东栋, 等. 18F-FDG PET/CT与PET/MRI在结直肠癌肝转移诊断中的比较分析[J]. 国际放射医学核医学杂志, 2021, 45(2): 75−82. DOI: 10.3760/cma.j.cn121381-202003009-00013.Yu J, Zhang Y, Ren DD, et al. Comparative analysis of 18F-FDG PET/CT and PET/MRI in the diagnosis of colorectal cancer liver metastases[J]. Int J Radiat Med Nucl Med, 2021, 45(2): 75−82. DOI: 10.3760/cma.j.cn121381-202003009-00013.
    [5] Martin O, Schaarschmidt BM, Kirchner J, et al. PET/MRI versus PET/CT for whole-body staging: results from a single-center observational study on 1, 003 sequential examinations[J]. J Nucl Med, 2020, 61(8): 1131−1136. DOI: 10.2967/jnumed.119.233940.
    [6] Morsing A, Hildebrandt MG, Vilstrup MH, et al. Hybrid PET/MRI in major cancers: a scoping review[J]. Eur J Nucl Med Mol Imaging, 2019, 46(10): 2138−2151. DOI: 10.1007/s00259-019-04402-8.
    [7] Haubold J, Demircioglu A, Gratz M, et al. Non-invasive tumor decoding and phenotyping of cerebral gliomas utilizing multiparametric 18F-FET PET-MRI and MR fingerprinting[J]. Eur J Nucl Med Mol Imaging, 2020, 47(6): 1435−1445. DOI: 10.1007/s00259-019-04602-2.
    [8] Evangelista L, Zattoni F, Cassarino G, et al. PET/MRI in prostate cancer: a systematic review and meta-analysis[J]. Eur J Nucl Med Mol Imaging, 2021, 48(3): 859−873. DOI: 10.1007/s00259-020-05025-0.
    [9] Rice TW, Patil DT, Blackstone EH. 8th edition AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice[J]. Ann Cardiothorac Surg, 2017, 6(2): 119−130. DOI: 10.21037/acs.2017.03.14.
    [10] Lee G, Hoseok I, Kim SJ, et al. Clinical implication of PET/MR imaging in preoperative esophageal cancer staging: comparison with PET/CT, endoscopic ultrasonography, and CT[J]. J Nucl Med, 2014, 55(8): 1242−1247. DOI: 10.2967/jnumed.114.138974.
    [11] Yamada I, Miyasaka N, Hikishima K, et al. Ultra-high-resolution MR imaging of esophageal carcinoma at ultra-high field strength (7.0T) ex vivo: correlation with histopathologic findings[J]. Magn Reson Imaging, 2015, 33(4): 413−419. DOI: 10.1016/j.mri.2014.11.005.
    [12] Wei Y, Wu S, Shi DP, et al. Oesophageal carcinoma: comparison of ex vivo high-resolution 3.0T MR imaging with histopathological findings[J/OL]. Sci Rep, 2016, 6: 35109[2021-02-21]. https://www.nature.com/articles/srep35109. DOI: 10.1038/srep35109.
    [13] Giganti F, Ambrosi A, Petrone MC, et al. Prospective comparison of MR with diffusion-weighted imaging, endoscopic ultrasound, MDCT and positron emission tomography-CT in the pre-operative staging of oesophageal cancer: results from a pilot study[J]. Br J Radiol, 2016, 89(1068): 20160087. DOI: 10.1259/bjr.20160087.
    [14] Yu CW, Chen XJ, Lin YH, et al. Prognostic value of 18F-FDG PET/MR imaging biomarkers in oesophageal squamous cell carcinoma[J]. Eur J Radiol, 2019, 120: 108671. DOI: 10.1016/j.ejrad.2019.108671.
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Comparative analysis of the application value of 18F-FDG PET/MRI and MRI in preoperative T, N staging of patients with esophageal cancer

    Corresponding author: Yunbo Li, 59199548@qq.com; 
  • 1. Department of Nuclear Medicine, the Second Affiliated Hospital of Air Force Medical University, Xi'an 710024, China
  • 2. Department of Nuclear Medicine, Shaanxi Provincial Cancer Hospital, Xi'an 710061, China
  • 3. Department of Nuclear Medicine, the Second Affiliated Hospital of Shanxi Medical University, Taiyuan 030001, China
  • Received Date: 2021-02-22
  • Available Online: 2022-03-25

Abstract:  Objective To compare the application value of 18F-fluorodeoxyglucose (FDG) PET/MRI and MRI in the preoperative T and N staging of patients with esophageal cancer. Methods The clinical and imaging data of 30 patients who underwent radical resection for esophageal cancer in the Second Affiliated Hospital of the Air Force Military Medical University from January 2018 to December 2019 were retrospectively analyzed. The sample included 25 males and 5 females, aged 42–77(62.9±8.0) years old. All patients underwent 18F-FDG PET/MRI examination within 2 weeks before operation, and the postoperative histopathological examination results were used as the “gold standard” for staging. The Kappa test was employed to evaluate the consistency of 18F-FDGPET/MRI and MRI in the preoperative T and N staging of patients with esophageal cancer and in postoperative histopathological staging. The staging accuracy was compared using the χ2 test, and the values of the maximum standardized uptake (SUVmax), mean standardized uptake (SUVmean), apparent diffusion coefficient minimum vaalue (ADCmin), and apparent diffusion coefficient mean value (ADCmean) of metastatic lymph nodes and benign lymph nodes were compared using independent sample t test. Results 18F-FDG PET/MRI and MRI showed strong consistency in the preoperative T staging and postoperative histopathological staging of patients with esophageal cancer (Kappa value=0.757, 0.698; both P<0.001). The accuracy rates of 18F-FDG PET/MRI and MRI in the diagnosis of preoperative T staging in patients with esophageal cancer were 83.3% (25/30) and 80.0% (24/30) respectively, with no significant difference (χ2=0.110, P>0.05). The diagnostic accuracy of 18F-FDG PET/MRI for preoperative N staging in patients with esophageal cancer was higher than that of MRI (76.7% (23/30) vs. 66.7% (20/30)), and the difference was statistically significant (χ2=11.273, P<0.01). The SUVmax and SUVmean values of the metastatic lymph nodes were higher than those of the benign lymph nodes (5.77±2.66 vs. 2.79±1.29 and 3.16±1.28 vs. 1.78±1.01, respectively), and the difference was statistically significant (t=6.39, 5.96; both P<0.001). Furthermore, the ADCmin of metastatic lymph nodes was lower than that of benign lymph nodes (1.02±0.33 vs. 1.20±0.24), and the difference was statistically significant (t=−3.81, P<0.001). In comparison, there was no statistical significance in the comparison of ADCmean (t=−1.52, P>0.05). Conclusions The value of 18F-FDG PET/MRI in the preoperative T staging of patients with esophageal cancer is comparable to that of MRI, while its diagnostic performance for preoperative N staging of patients with esophageal cancer is better than MRI. Thus, it can be considered the preferred non-invasive preoperative staging method for patients with esophageal cancer.

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  • 食管癌是最常见的消化道恶性肿瘤之一，排在全球癌症相关病死的第6位[1]。早期手术切除是食管癌的主要治疗方法，术前准确分期对于患者治疗方案的制定及预后至关重要。目前常用的分期方法为CT和超声内镜检查，超声内镜可精确显示食管壁的结构，但其为有创检查，且易受操作者技术的影响；CT的软组织分辨率低，故其诊断的准确率亦较低。MRI的软组织分辨率高，具有多序列成像的优点，可清晰显示食管壁的各层结构，且随着成像方式和设备技术的进步，心跳、呼吸及食管蠕动等磁敏感伪影对图像质量的影响均明显减少[2]。据报道，MRI在食管癌患者T分期中的效能优于其他影像学检查[3]。18F-FDG PET/MRI将PET代谢显像与高组织对比度的MRI相结合，二者联合检测在肿瘤分期中有明显优势[4-5]。PET/MRI自2011年应用于临床以来，多用于脑部及盆腔肿瘤的成像[6-8]，目前国内外对PET/MRI应用于食管癌患者术前分期的研究报道极少。本研究回顾性分析30例行食管癌根治术患者的临床资料与影像学资料，对比分析18F-FDG PET/MRI和MRI在食管癌患者术前T、N分期中的应用价值。

    • 1.   资料与方法

      1.1.   一般资料

    • 回顾性分析2018年1月至2019年12月于空军军医大学第二附属医院行食管癌根治术的30例患者的临床资料与影像学资料，其中男性25例、女性5例，年龄42~77（62.9±8.0）岁。纳入标准：（1）经胃镜活检的组织病理学检查确诊为食管癌且无远处转移；（2）行食管癌根治术，至少对7个淋巴结进行组织病理学检查；（3）术前2周内行18F-FDG PET/MRI检查；（4）签署了知情同意书。排除标准：（1）有高场强MRI禁忌证或幽闭恐惧症；（2）术前接受过放化疗；（3）合并严重慢性病或有严重肝肾功能损害；（4）合并远处转移或有其他手术禁忌证。本研究符合《赫尔辛基宣言》的原则。

      • 1.2.   显像方法

    • 采用德国西门子公司Biograph mMR PET/MR一体机（MRI 3.0T）进行显像。显像剂为18F-FDG，由南京江原安迪科正电子研究发展有限公司提供，放射化学纯度>95%。患者需禁食6 h以上，空腹血糖水平<11.2 mmol/L，安静状态下经肘静脉注射18F-FDG（3.7 MBq/kg），剂量为（222.71±32.78） MBq，视听封闭休息40 min后行18F-FDG PET/MRI扫描。图像采集方式为静态采集，扫描范围从颅底至股骨上1/3，扫描方式为容积扫描。PET与MRI同步扫描，MRI扫描条件如下。（1）T1加权成像三维容积内插体部序列（VIBE）横断面扫描：重复时间 4.04 ms、回波时间 1.24 ms、层厚3.2 mm、层距0 mm、视野 420 mm×320 mm、矩阵320×175；（2）T2加权成像半傅里叶采集单次激发快速自旋回波序列（HASTE）冠状面扫描：重复时间 1000 ms、回波时间 95 ms、层厚6 mm、层距1.2 mm、视野400 mm×400 mm、矩阵256×256；（3）T2加权成像刀锋伪影校正脂肪抑制（Blade fs）频率衰减反转恢复序列（SPAIR）横断面扫描：重复时间 2200 ms、回波时间 86 ms、层厚6 mm、层距0 mm、视野400 mm×400 mm、矩阵320×320；（4）扩散加权成像（diffusion weighted imaging，DWI）平面回波成像序列（EPI）扫描：b值为50、1000 s/mm2，重复时间6400 ms、回波时间78 ms、层厚6 mm、层距0 mm、视野400 mm×300 mm、矩阵128×96，自动生成表观扩散系数（apparent diffusion coefficient，ADC）图。PET扫描条件：衰减校正采用三维容积内插体部检查水脂分离技术梯度回波序列（VIBE DIXON），层厚2 mm、高清重建、迭代次数2、矩阵172×172、放大倍数1.0、半峰全宽2.0、散射校正为相对校正。

      • 1.3.   图像分析

    • PET/MRI图像由2位中级以上职称的核医学科医师独立阅片，MRI图像由2位中级以上职称的放射科医师独立阅片，意见不一致时分别与2位高级职称核医学科或放射科医师商议后确定最终结果。采用MIMvista 6.5后处理工作站（北京明维视景医疗软件开发有限公司）获得MRI、PET及PET/MRI融合图像。参考T2加权成像序列图像中显示淋巴结最大界面的层面，在DWI序列图像高信号区勾画ROI，并复制ROI至ADC图的相应区域，获得相应淋巴结的ADC最小值（ADC minimum value，ADCmin）和ADC平均值（ADC mean value，ADCmean）；PET图像以纵隔血池本底SUVmax为临界值确定淋巴结边界以勾画ROI，记录相应淋巴结的SUVmax和平均SUV（mean standardized uptake value，SUVmean）。

      • 1.4.   诊断标准

    • 参照2017年第8版美国癌症联合委员会/国际抗癌联盟的食管癌和食管胃结合部癌分期标准[9]对患者进行分期，以转移性淋巴结的数目作为N分期标准，N0期：无区域淋巴结转移；N1期：1~2个区域淋巴结转移；N2期：3~6个区域淋巴结转移；N3期：≥7个区域淋巴结转移。MRI对食管癌患者T分期的诊断标准如下，T1~T2期：病灶周围肌层可见完整的线状低至中等信号；T3期：病灶周围肌层的线状低至中等信号中断或消失，脂肪间隙清晰；T4期：病灶与邻近结构之间的脂肪间隙消失，并伴邻近结构受侵征象。MRI表现为淋巴门结构不清，边缘不规则或内部信号不均匀，DWI呈高信号，符合其一且不论淋巴结的长径大小均诊断为转移性淋巴结。PET图像在食管癌患者的T分期中不作为参考。PET对食管癌患者转移性淋巴结的诊断标准：SUVmax>纵隔血池SUVmax。以上述PET的诊断标准结合MRI的诊断标准作为PET/MRI对食管癌患者转移性淋巴结的诊断标准。

      • 1.5.   统计学方法

    • 应用SPSS 25.0软件进行统计学分析。18F-FDG PET/MRI和MRI对食管癌患者术前T、N分期的诊断效能采用Kappa检验进行一致性评估，Kappa值<0为二者不一致；0≤Kappa值≤0.2为二者的一致性较差；0.2<Kappa值≤0.4为二者的一致性一般；0.4<Kappa值≤0.6为二者的一致性中等；0.6<Kappa值≤0.8为二者的一致性较强；0.8<Kappa值≤1为二者的一致性强。18F-FDG PET/MRI与MRI对食管癌患者术前T、N分期准确率的比较采用χ2检验。符合正态分布的数据以$\bar x \pm s $表示，转移性淋巴结与良性淋巴结参数的比较采用独立样本t检验（方差齐）。P<0.05为差异有统计学意义。

    2.   结果

      2.1.   临床资料的比较

    • 术前行18F-FDG PET/MRI检查的30例食管癌患者中，发现结肠占位1例，进一步行结肠镜和组织病理学检查确诊为结肠癌，同时行食管癌及结肠癌根治术；其余29例患者行食管癌根治术。术中发现食管癌原发灶位于食管上段1例、中段15例、下段11例、食管胃结合部3例。术后组织病理学检查结果显示，30例食管癌患者中，T1期3例、T2期4例、T3期14例、T4期9例；N0期16例、N1期6例、N2期7例、N3期1例；鳞癌26例、腺癌4例。

      • 2.2.   18F-FDG PET/MRI与MRI对食管癌患者术前T分期的诊断效能比较

    • 18F-FDG PET/MRI与MRI在食管癌患者术前T分期和术后组织病理学分期的一致性均较强（Kappa值=0.757、0.698，均P<0.001）；18F-FDG PET/MRI和MRI对食管癌患者术前T分期的诊断准确率分别为83.3%（25/30）、80.0%（24/30），二者的差异无统计学意义（χ2=0.110，P=0.740）。具体T分期情况见表1。T1~T4期食管癌患者的典型18F-FDG PET/MRI影像学表现见图1。

      术后组织病理
      学分期      		18F-FDG PET/MRI分期MRI分期
      T1~T2期T3期T4期T1~T2期T3期T4期
      T1~T2期（n=7） 7 0 0 7 0 0
      T3期（n=14） 1 10 3 1 9 4
      T4期（n=9） 0 1 8 0 1 8
      注：FDG为氟脱氧葡萄糖；PET为正电子发射断层显像术；MRI为磁共振成像

      Table 1.  Comparison of 18F-FDG PET/MRI and MRI in preoperative T staging and postoperative histopathological staging in patients with esophageal cancer (case)

      Figure 1.  18F-FDG PET/MRI cross-sectional images of patients with T1−T4 stage esophageal cancer

      • 2.3.   18F-FDG PET/MRI与MRI对食管癌患者术前N分期的诊断效能比较

    • 18F-FDG PET/MRI对食管癌患者术前N分期与术后组织病理学分期的一致性较强（Kappa值=0.640，P<0.001），MRI对食管癌患者术前N分期与术后组织病理学的一致性中等（Kappa值=0.477，P<0.001）。18F-FDG PET/MRI和MRI诊断对食管癌患者术前N分期的诊断准确率分别为76.7%（23/30）、66.7%（20/30），且差异有统计学意义（χ2=11.273，P=0.001）。具体N分期情况见表2。

      术后组织病
      理学分期      		18F-FDG PET/MRI分期MRI分期
      N0期N1期N2期N3期N0期N1期N2期N3期
      N0期（n=16） 12 2 1 1 13 2 0 1
      N1期（n=6） 2 4 0 0 2 3 1 0
      N2期（n=7） 0 1 6 0 0 2 4 1
      N3期（n=1） 0 0 0 1 0 0 1 0
      注：FDG为氟脱氧葡萄糖；PET为正电子发射断层显像术；MRI为磁共振成像

      Table 2.  Comparison of 18F-FDG PET/MRI and MRI in preoperative N staging and postoperative histopathological staging in patients with esophageal cancer (case)

      • 2.4.   转移性淋巴结和良性淋巴结的18F-FDG PET/MRI半定量参数比较

    • 共对30例食管癌患者的282个淋巴结进行组织病理学检查，其中37个淋巴结明确为转移性淋巴结（18F-FDG PET/MRI检出34个），245个淋巴结明确为良性淋巴结（18F-FDG PET/MRI检出192个）。由表3可知，转移性淋巴结的SUVmax和SUVmean均明显高于良性淋巴结，且差异均有统计学意义（均P<0.001）；转移性淋巴结的ADCmin较良性淋巴结低，且差异有统计学意义（P<0.001），转移性淋巴结与良性淋巴结ADCmean的比较，差异无统计学意义（P>0.05）。

      组别SUVmaxSUVmeanADCminADCmean
      转移性淋巴结（n=34） 5.77±2.66 3.16±1.28 1.02±0.33 1.42±0.22
      良性淋巴结（n=192） 2.79±1.29 1.78±1.01 1.20±0.24 1.48±0.29
      t值 6.39 5.96 −3.81 −1.52
      P值 <0.001 <0.001 <0.001 0.133
      注：FDG为氟脱氧葡萄糖；PET为正电子发射断层显像术；MRI为磁共振成像；SUVmax为最大标准化摄取值；SUVmean为平均标准化摄取值；ADCmin为表观弥散系数最小值；ADCmean为表观弥散系数平均值

      Table 3.  Comparison of 18F-FDG PET/MRI semiquantitative parameters in metastatic and benign lymph nodes of 30 patients with esophageal cancer ($\bar x \pm s $)

    3.   讨论

    • 本研究结果显示，18F-FDG PET/MRI和MRI对食管癌患者术前T分期与术后组织病理学分期的一致性均较强，二者对食管癌患者术前T分期的诊断价值相当；在N分期中，18F-FDG PET/MRI的诊断准确率高于MRI。在转移性淋巴结和良性淋巴结的18F-FDG PET/MRI半定量参数的对比分析中，转移性淋巴结的SUVmax和SUVmean均明显高于良性淋巴结，ADCmin较良性淋巴结低。

      本研究中，18F-FDG PET/MRI对食管癌患者术前T分期的诊断准确率为83.3%。Lee等[10]将15例食管癌患者的术前18F-FDG PET/MRI分期结果与术后组织病理学分期结果进行对比，结果显示，18F-FDG PET/MRI对食管癌患者术前T分期的诊断准确率为86.7%（13/15），与本研究结果基本一致。由于PET显像的空间分辨率较低，故对食管壁浸润程度的判断主要依靠MRI。Yamada等[11]和Wei等[12]对离体的食管癌组织进行MRI成像，结果显示，MRI评估食管壁浸润程度的准确率均达90%以上。本研究中18F-FDG PET/MRI对食管癌患者T分期的诊断准确率低于上述两项研究，究其原因，可能是因为18F-FDG PET/MRI的扫描时间较长，且易受呼吸、心跳及食管蠕动等磁敏感伪影的影响，而离体的食管癌组织不受以上运动伪影的干扰。本研究18F-FDG PET/MRI在食管癌患者术前T分期中有3例T3期患者被高估，1例T3期患者和1例T4期患者被低估，这与食管壁局部的炎症渗出及纤维化导致的18F-FDG PET/MRI中病灶与周围组织的分界清晰度降低有关。

      本研究结果显示，18F-FDG PET/MRI对食管癌患者术前N分期的诊断准确率高于MRI。Giganti等[13]对18例食管癌患者进行研究，结果显示，1.5T MRI结合DWI对食管癌患者术前N分期的诊断准确率为66%。转移性淋巴结的MRI信号缺乏特异性，尤其是MRI对长径较小的食管旁淋巴结显示欠佳。本研究以边缘不规则或内部信号不均匀、DWI呈高信号，结合18F-FDG PET半定量参数SUVmax>纵隔血池SUVmax作为转移性淋巴结的诊断标准，结果显示，18F-FDG PET/MRI对食管癌患者术前N分期的诊断准确率为76.7%，高于单独行MRI进行分期的诊断准确率。Lee等[10]报道，与超声内镜、CT和18F-FDG PET/CT相比，18F-FDG PET/MRI对食管癌患者术前N分期的诊断效能最高，与本研究结果相似。Yu等[14]的研究结果显示，食管癌原发灶的18F-FDG PET/MRI代谢参数在预测食管鳞癌的淋巴结转移中具有一定价值。以上结果表明，MRI多序列成像结合PET代谢信息可提高对食管癌患者术前N分期的诊断准确率。

      本研究中我们还发现，食管癌患者转移性淋巴结的SUVmax和SUVmean均明显高于良性淋巴结，ADCmin较良性淋巴结低。半定量参数SUVmax与SUVmean可反映组织细胞的代谢特征，一般来说，恶性肿瘤的生长速度快，葡萄糖的利用率高，从而呈现出较高的SUV。ADC值可通过细胞中水分子的弥散受限程度反映肿瘤细胞的特征。然而炎症淋巴结与转移性淋巴结的SUV和ADC值均存在一定程度的交叉，故18F-FDG PET/MRI对转移性淋巴结的诊断存在漏诊和误诊的问题。本研究中3个经术后组织病理学检查证实的转移性淋巴结未被18F-FDG PET/MRI检出，究其原因，可能是受累淋巴结为癌旁淋巴结，其被高代谢的原发灶所掩盖；另外，当转移性淋巴结较小（长径<3 mm）时，MRI则无法分辨；且若肿瘤负荷低，则处于增殖周期的肿瘤细胞少，PET显像中亦未呈现异常代谢，也可导致假阴性结果。部分增殖性病变及炎症也含有代谢旺盛的细胞，从而易导致假阳性结果。故临床中判断转移性淋巴结不能单纯依靠SUV，须结合ADC值及其他信息综合分析。

      本研究尚存在一些不足之处：（1）本研究为回顾性分析，研究结果可能存在选择偏倚；（2）由于伴远处转移的食管癌患者多数未经组织病理学检查证实，故本研究未纳入伴远处转移的食管癌患者，以致未能分析18F-FDG PET/MRI对食管癌患者术前M分期的诊断效能；（3）由于条件限制，本研究的成像方式为常规18F-FDG PET/MRI扫描，未使用对比剂进行增强扫描，无法对T1期与T2期的病灶进行精确区分，故将T1、T2期合并分析，后续研究中若有条件将使用动态增强MRI，为食管癌患者提供更精准的分期信息；（4）使用的PET/MRI应用于临床的时间尚短，且检查费用高昂，符合条件的病例数有限，需在后期研究中扩大样本量进一步验证。

      综上所述，18F-FDG PET/MRI在食管癌原发灶浸润程度诊断中的价值与MRI相当，但其对食管癌转移性淋巴结的诊断有明确优势。因此，18F-FDGPET/MRI在食管癌患者术前T、N分期中具有较好的应用前景，值得在临床中推广应用。

      利益冲突　所有作者声明无利益冲突

      作者贡献声明　惠金子负责研究的设计与实施、数据的采集、论文的撰写；王磊负责数据的统计分析与解释；赵德善负责论文的审阅；袁梦晖、魏龙晓负责论文的技术材料支持；李云波负责论文的修改、最终版本的修订；许建林、施常备负责论文的指导

Reference (14)

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