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肾透明细胞癌(clear cell renal cell carcinoma,ccRCC)是肾细胞癌最常见的组织病理学类型,约占肾癌的75%~87%,早期常无症状。随着检查手段的不断提高和体检筛查的普及,越来越多的早期肾癌,尤其是T1期肾癌的检出率逐渐升高。目前最常用的肾癌分期为美国泌尿协会2009年制定的第7版肾癌分级系统[1],其中T1期肾癌指肿瘤最大径≤7 cm,其组织病理学分级(Fuhrman分级)为临床应用最为广泛的分级[2],该系统以细胞核大小、形态和核仁突出为基础进行肾癌Ⅰ ~Ⅳ级的区分。既往研究结果证实Fuhrman组织病理学分级是判断肾癌恶性程度、预测肿瘤侵袭性和复发转移的重要指标[2-4]。同时该分级系统对术后诊断,早期、准确地进行肾癌术前恶性程度的预测,治疗方案的选择和预后评估具有重要意义。本研究收集具有完整临床资料且经术后组织病理学检查确诊的66例T1期ccRCC患者的多层螺旋CT(multi-slice CT,MSCT)资料,分析其CT征象和强化特征参数,探讨术前预测不同Fuhrman组织病理学分级的可行性。
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对照术后的Fuhrman组织病理学分级,66例T1期ccRCC患者中,低级别组36例,其中男性27例、女性9例,年龄 (58.0±14.1)岁;高级别组30例,其中男性13例、女性17例,年龄(59.3±16.1)岁。2组患者发病年龄的差异无统计学意义(t=−0.357,P=0.722),男性的发病率高于女性(χ2=6.873,P=0.009)。2名医师对MSCT的术前评估与Fuhrman组织病理学分级的一致性较好(Kappa=0.940,P<0.001)。
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以Fuhrman组织病理学分级作为“金标准”,低级别组和高级别组患者的MSCT表现在肿瘤形态、最大径、内部结构(囊变、坏死)、分叶征、假包膜、包膜侵犯以及肿瘤强化均匀度的差异均有统计学意义(均P<0.05);肿瘤部位、生长方式、生长部位、边界、交界面、肾窦侵犯、强化程度的差异均无统计学意义(均P>0.05,表1)。
项目 低级别组(n=36) 高级别组(n=30) 检验值 P值 肿瘤部位 χ2=0.051 0.822 左肾 17 15 右肾 19 15 肿瘤形态 − <0.001 圆形/类圆形 36 15 不规则型 0 15 生长方式 χ2=0.292 0.589 内生型 18 17 外生型 18 13 生长部位 χ2=0.786 0.692 肾上极 9 5 肾中极 12 10 肾下极 15 15 边界 − 0.327 清楚 7 3 模糊 29 27 最大径(cm) 30.34±9.39 42.32±20.82 t=−2.916 0.006 内部结构 囊变 24 9 χ2=8.800 0.006 坏死 5 26 − <0.001 钙化 0 1 − 0.455 出血 0 3 − 0.089 均无 7 2 − 0.166 分叶征 − 0.001 无 33 17 有 3 13 浅分叶 3 9 − 0.529 深分叶 0 4 假包膜 χ2=7.830 0.007 有 22 8 无 14 22 交界面 χ2=0.894 0.344 ≤90° 21 14 >90° 15 16 包膜侵犯 − 0.013 有 29 30 无 7 0 肾窦侵犯 χ2=3.732 0.077 有 18 22 无 18 8 强化均匀度 − 0.013 均匀 7 0 不均匀 29 30 强化程度 − 0.620 明显强化 33 29 弱强化 3 1 注:CT为计算机体层摄影术;−表示Fisher确切概率法 表 1 不同Fuhrman组织病理学分级肾透明细胞癌患者的多层螺旋CT征象比较
Table 1. Comparison of multislice spiral CT findings in patients with clear cell renal cell carcinoma of different Fuhrman histopathological grades
不同Fuhrman组织病理学分级患者有统计学意义的MSCT征象中,肿瘤形态预测高级别Fuhrman组织病理学分级患者的特异度(100%)和阳性预测值(100%)最高;包膜侵犯和强化不均匀度预测高级别Fuhrman组织病理学分级的灵敏度(100%和100%)最高;坏死和分叶征预测高级别Fuhrman组织病理学分级的特异度(86.1% 和91.7%)和准确率(86.4% 和69.7%)均较高(表2)。采用多因素Logistic回归分析校正,结果表明,假包膜是Fuhrman组织病理学分级的独立预测因素(OR=0.082,95%CI:0.007~0.908,P=0.041)。
CT征象 灵敏度 特异度 阳性预测值 阴性预测值 准确率 肿瘤形态 50.0(15/30) 100.0(36/36) 100.0(15/15) 70.6(36/51) 77.3(51/66) 囊变 30.0(9/30) 33.3(12/36) 27.3(9/33) 36.4(12/33) 31.8(21/66) 坏死 86.7(26/30) 86.1(31/36) 83.9(26/31) 88.6(31/35) 86.4(57/66) 分叶征 43.3(13/30) 91.7(33/36) 81.3(13/16) 66.0(33/50) 69.7(46/66) 假包膜 26.7(8/30) 38.9(14/36) 26.7(8/30) 38.9(14/36) 33.3(22/66) 包膜侵犯 100.0(30/30) 19.4(7/36) 50.8(30/59) 100.0(7/7) 56.1(37/66) 强化不均匀度 100.0(30/30) 19.4(7/36) 50.8(30/59) 100.0(7/7) 56.1(37/66) 注:CT为计算机体层摄影术 表 2 CT阳性征象对高Fuhrman组织病理学分级肾透明细胞癌患者的诊断效能(%)
Table 2. Diagnostic efficacy of CT positive signs in patients with clear cell renal cell carcinoma with high Fuhrman histopathological grades (%)
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低级别组患者的皮髓质期病灶CT值、CT差值、增强比值、增强指数均高于高级别组,且差异均有统计学意义(均P<0.05),其余指标的差异均无统计学意义(均P>0.05,表3)。以Fuhrman组织病理学分级作为分级诊断“金标准”,皮髓质期病灶CT值、CT差值、增强比值、增强指数的ROC曲线的AUC分别为0.849(95% CI:0.744~0.953,P<0.001)、0.848(95% CI:0.748~0.948,P<0.001)、0.741(95% CI:0.621~0.861,P<0.001)、0.757(95% CI:0.637~0.878,P<0.001)。
项目 低级别组(n=36) 高级别组(n=30) t值 P值 平扫期病灶CT值(HU) 35.11±9.09 37.50±10.20 −1.005 0.319 皮髓质期病灶CT值(HU) 169.03±36.50 132.90±16.28 5.017 <0.001 实质期病灶CT值(HU) 113.50±35.28 116.67±16.20 −0.389 0.698 排泄期病灶CT值(HU) 82.81±23.12 89.81±19.42 −1.229 0.224 皮髓质期病灶CT差值(HU) 133.92±37.31 95.40±19.84 5.082 <0.001 实质期病灶CT差值(HU) 78.39±36.09 79.17±31.67 −0.092 0.927 皮髓质期病灶增强比值 4.09±1.61 2.79±1.09 3.751 <0.001 实质期病灶增强比值 2.42±1.41 2.36±1.40 0.187 0.853 肾脏皮髓质期增强比值 3.40±1.41 3.81±1.51 −1.144 0.257 肾脏实质期增强比值 3.19±1.08 3.48±1.31 −0.966 0.338 皮髓质期病灶增强指数 1.45±1.13 0.91±0.81 2.180 0.033 实质期病灶增强指数 0.77±0.38 0.71±0.36 0.680 0.499 注:CT为计算机体层摄影术 表 3 不同Fuhrman组织病理学分级肾透明细胞癌患者各期CT值及其强化参数的对比(
)$\bar{x} \pm s $ Table 3. Comparison of CT value and enhancement parameters in different stages of clear cell renal cell carcinoma patients with different Fuhrman histopathological grades (
)$\bar{x} \pm s $ 皮髓质期病灶CT值和CT差值对于不同级别Fuhrman组织病理学分级患者具有较高的诊断效能,皮髓质期病灶CT值的最佳临界值为152.5 HU(灵敏度为80.6%、特异度为93.3%、约登指数为0.739)。皮髓质期病灶CT值≤152.5 HU的患者共35例,其中高级别组28例(80.0%)。皮髓质期病灶CT差值的最佳临界值为120.5 HU(灵敏度为72.2%、特异度为93.3%、约登指数为0.655)。皮髓质期病灶CT差值≤120.5 HU的患者共31例,其中高级别组28例(90.3%)。皮髓质期病灶增强比值的最佳临界值为3.356(灵敏度为63.9%、特异度为80.0%、约登指数为0.439)。皮髓质期病灶增强比值≤3.356的患者共37例,其中高级别组24例(64.9%)。皮髓质期病灶增强指数的最佳临界值为0.953(灵敏度为77.8%、特异度为70.0%、约登指数为0.478)。皮髓质期增强指数≤0.953的患者共29例,其中高级别组21例(72.4%)(图1)。
MSCT征象及强化参数预测T1期肾透明细胞癌Fuhrman组织病理学分级
MSCT findings and enhancement parameters analysis of the prediction of Fuhrman pathological grading in stage T1 clear cell renal cell carcinoma
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摘要:
目的 探讨多层螺旋CT(MSCT)征象及强化参数预测T1期肾透明细胞癌 (ccRCC)的Fuhrman组织病理学分级。 方法 回顾性分析2014年1月至2021年3月于江苏大学附属昆山医院经术后组织病理学检查确诊为T1期ccRCC的66例患者的临床资料和影像学资料,其中男性40例、女性26例,年龄(58.3±14.9)岁。所有患者依据Fuhrman组织病理学分级,分为低级别组(Ⅰ~Ⅱ级)和高级别组(Ⅲ~Ⅳ级),分析2组患者的MSCT平扫和增强图像,比较2组患者的MSCT征象及其强化参数的差异,分析观察指标的预测效能。符合正态分布的计量资料的组间比较采用t检验;计数资料的组间比较采用卡方检验或Fisher确切概率法;采用Kappa检验比较2名医师测量结果的一致性;以Fuhrman组织病理学分级为“金标准”,绘制受试者工作特征(ROC)曲线,计算曲线下面积(AUC);采用二元多因素Logistic回归分析评估影响ccRCC Fuhrman组织病理学分级的独立危险因素。 结果 2组患者的MSCT表现在肿瘤形态、内部结构(囊变、坏死)、分叶征、假包膜、包膜侵犯、肿瘤强化均匀度的差异均有统计学意义(Fisher确切概率法,χ2=8.800、7.830,均P<0.05)。低级别组患者皮髓质期病灶的CT值、CT差值、增强比值、增强指数均高于高级别组[(169.03±36.50) HU vs. (132.90±16.28) HU、(133.92±37.31) HU vs. (95.40±19.84) HU、4.09±1.61 vs. 2.79±1.09、1.45±1.13 vs. 0.91±0.81],且差异均有统计学意义(t=2.180~5.082,均P<0.05),4项指标的AUC分别为0.849(95%CI:0.744~0.953,P<0.001)、0.848(95%CI:0.748~0.948,P<0.001)、0.741(95%CI:0.621~0.861,P<0.001)、0.757(95%CI:0.637~0.878,P<0.001),最佳临界值分别为152.5 HU、120.5 HU、3.356、0.953,约登指数分别为0.739、0.655、0.439、0.478。多因素Logistic回归分析结果表明,假包膜是Fuhrman组织病理学分级的独立预测因素(OR=0.082,95%CI:0.007~0.908,P<0.05)。 结论 ccRCC患者平扫和增强MSCT图像的表现多样,结合皮髓质期肿瘤病灶CT值、CT差值、增强比值和增强指数,有助于预测Fuhrman组织病理学分级。其中,假包膜可以作为独立预测因素。 -
关键词:
- 癌,肾细胞 /
- 体层摄影术,螺旋计算机 /
- 征象 /
- 强化特征 /
- Fuhrman病理分级
Abstract:Objective To investigate the prediction of Fuhrman histopathological grade of T1 clear cell renal cell carcinoma (ccRCC) by multi-slice computed tomography (MSCT) signs and enhancement parameters. Methods The clinical and imaging data of 66 patients with T1 stage ccRCC diagnosed by postoperative histopathology in Kunshan Hospital Affiliated to Jiangsu University from January 2014 to March 2021, including 40 males and 26 females, aged (58.3±14.9) years, were analyzed retrospectively. All patients were divided into low-(Ⅰ −Ⅱ) and high-grade group (Ⅲ−Ⅳ) in accordance with the Fuhrman histopathological classification. The plain and enhanced images of MSCT of the patients in the two groups were analyzed, and the differences in MSCT signs and enhancement parameters between the two groups were compared. The predictive effectiveness of the observation indicators was analyzed. T-test was used to compare the measurement data with normal distribution; Chi square test or Fisher's exact test was used to compare the counting data between groups; Kappa test was used to compare the consistency of measurement results between two physicians. The "gold standard" was Fuhrman histopathological grading. The receiver operating characteristic curve was drawn, and area under curve (AUC) was calculated. Independent risk factors were evaluated by binary Logistic regression analysis. Results The MSCT findings of the two groups were statistically significant in terms of tumor morphology, internal structure (cystic degeneration and necrosis), lobulation sign, pseudocapsule, capsule invasion, and tumor enhancement homogeneity (Fisher's exact test, χ2=8.800, 7.830; all P<0.05). The CT value, CT difference, enhancement ratio, and enhancement index of tumor focus in the low-grade group were higher than those in the high-grade group ((169.03±36.50) HU vs. (132.90±16.28) HU, (133.92±37.31) HU vs. (95.40±19.84) HU, 4.09±1.61 vs. 2.79±1.09, 1.45±1.13 vs. 0.91±0.81, respectively), and the difference was statistically significant (t=2.180−5.082, all P<0.05). The AUC of the four MSCT enhancements parameters were 0.849 (95%CI: 0.744–0.953, P<0.001), 0.848 (95%CI: 0.748–0.948, P<0.001), 0.741 (95%CI: 0.621–0.861, P<0.001), and 0.757 (95%CI: 0.637–0.878, P<0.001), the optimal critical values were 152.5 HU, 120.5 HU, 3.356, and 0.953, respectively. The Yoden indexes were 0.739, 0.655, 0.439 and 0.478. Multivariate Logistic regression analysis results show that pseudocapsule was an independent predictor of Fuhrman histopathological grading (OR=0.082, 95%CI: 0.007–0.908, P<0.05). Conclusions The manifestations of plain and enhanced MSCT images of ccRCC are diverse. Combined with the CT value, CT difference, enhancement ratio, and enhancement index of tumor lesions in the corticomedullary phase are helpful in the prediction of Fuhrman histopathological grading. Pseudocapsules can be used as an independent predictor. -
表 1 不同Fuhrman组织病理学分级肾透明细胞癌患者的多层螺旋CT征象比较
Table 1. Comparison of multislice spiral CT findings in patients with clear cell renal cell carcinoma of different Fuhrman histopathological grades
项目 低级别组(n=36) 高级别组(n=30) 检验值 P值 肿瘤部位 χ2=0.051 0.822 左肾 17 15 右肾 19 15 肿瘤形态 − <0.001 圆形/类圆形 36 15 不规则型 0 15 生长方式 χ2=0.292 0.589 内生型 18 17 外生型 18 13 生长部位 χ2=0.786 0.692 肾上极 9 5 肾中极 12 10 肾下极 15 15 边界 − 0.327 清楚 7 3 模糊 29 27 最大径(cm) 30.34±9.39 42.32±20.82 t=−2.916 0.006 内部结构 囊变 24 9 χ2=8.800 0.006 坏死 5 26 − <0.001 钙化 0 1 − 0.455 出血 0 3 − 0.089 均无 7 2 − 0.166 分叶征 − 0.001 无 33 17 有 3 13 浅分叶 3 9 − 0.529 深分叶 0 4 假包膜 χ2=7.830 0.007 有 22 8 无 14 22 交界面 χ2=0.894 0.344 ≤90° 21 14 >90° 15 16 包膜侵犯 − 0.013 有 29 30 无 7 0 肾窦侵犯 χ2=3.732 0.077 有 18 22 无 18 8 强化均匀度 − 0.013 均匀 7 0 不均匀 29 30 强化程度 − 0.620 明显强化 33 29 弱强化 3 1 注:CT为计算机体层摄影术;−表示Fisher确切概率法 表 2 CT阳性征象对高Fuhrman组织病理学分级肾透明细胞癌患者的诊断效能(%)
Table 2. Diagnostic efficacy of CT positive signs in patients with clear cell renal cell carcinoma with high Fuhrman histopathological grades (%)
CT征象 灵敏度 特异度 阳性预测值 阴性预测值 准确率 肿瘤形态 50.0(15/30) 100.0(36/36) 100.0(15/15) 70.6(36/51) 77.3(51/66) 囊变 30.0(9/30) 33.3(12/36) 27.3(9/33) 36.4(12/33) 31.8(21/66) 坏死 86.7(26/30) 86.1(31/36) 83.9(26/31) 88.6(31/35) 86.4(57/66) 分叶征 43.3(13/30) 91.7(33/36) 81.3(13/16) 66.0(33/50) 69.7(46/66) 假包膜 26.7(8/30) 38.9(14/36) 26.7(8/30) 38.9(14/36) 33.3(22/66) 包膜侵犯 100.0(30/30) 19.4(7/36) 50.8(30/59) 100.0(7/7) 56.1(37/66) 强化不均匀度 100.0(30/30) 19.4(7/36) 50.8(30/59) 100.0(7/7) 56.1(37/66) 注:CT为计算机体层摄影术 表 3 不同Fuhrman组织病理学分级肾透明细胞癌患者各期CT值及其强化参数的对比(
)$\bar{x} \pm s $ Table 3. Comparison of CT value and enhancement parameters in different stages of clear cell renal cell carcinoma patients with different Fuhrman histopathological grades (
)$\bar{x} \pm s $ 项目 低级别组(n=36) 高级别组(n=30) t值 P值 平扫期病灶CT值(HU) 35.11±9.09 37.50±10.20 −1.005 0.319 皮髓质期病灶CT值(HU) 169.03±36.50 132.90±16.28 5.017 <0.001 实质期病灶CT值(HU) 113.50±35.28 116.67±16.20 −0.389 0.698 排泄期病灶CT值(HU) 82.81±23.12 89.81±19.42 −1.229 0.224 皮髓质期病灶CT差值(HU) 133.92±37.31 95.40±19.84 5.082 <0.001 实质期病灶CT差值(HU) 78.39±36.09 79.17±31.67 −0.092 0.927 皮髓质期病灶增强比值 4.09±1.61 2.79±1.09 3.751 <0.001 实质期病灶增强比值 2.42±1.41 2.36±1.40 0.187 0.853 肾脏皮髓质期增强比值 3.40±1.41 3.81±1.51 −1.144 0.257 肾脏实质期增强比值 3.19±1.08 3.48±1.31 −0.966 0.338 皮髓质期病灶增强指数 1.45±1.13 0.91±0.81 2.180 0.033 实质期病灶增强指数 0.77±0.38 0.71±0.36 0.680 0.499 注:CT为计算机体层摄影术 -
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