肝良恶性肿瘤包膜回缩征影像表现及其病理基础欧幼宽, 等 1133 smooth or rough for the edge of capsular retraction was significant difference between the ben

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1 1132 中南大学学报 ( 医学版 ) J Cent South Univ (Med Sci) 2015, 40(10) DOI: /j.issn 肝良恶性肿瘤包膜回缩征影像表现及其病理基础欧幼宽 1,2, 肖恩华 1, 尚全良 1 1, 陈娟 (1. 中南大学湘雅二医院放射科, 长沙 ;2. 福建省晋江市医院影像科, 福建晋江 ) [ 摘要 ] 目的 : 探讨肝良恶性肿瘤引起包膜回缩征的 CT 和 MRI 表现及其病理基础方法 : 回顾性分析经病理证实的 50 例肝良恶性肿瘤肝包膜回缩征的 CT 和 MRI 表现及病理特点通过影像归档和通信系统观察比较包膜下肝良恶性肿瘤形态大小及肝包膜回缩宽度深度边缘情况肝包膜下是否有积液的异同, 显微镜下分析肿瘤内部及周围结构分化程度及纤维组织增生量结果 : 肝恶性肿瘤 44 例, 良性肿瘤 6 例良性肿瘤与高中低三个不同分化等级的恶性肿瘤肝包膜回缩边缘光整或毛糙差异有统计学意义 ( 均 P<0.05) 纤维组织增生量不同的肿瘤肝包膜回缩宽度深度差异有统计学意义 ( 均 P<0.05) 肿瘤直径大小与肝包膜回缩宽度深度呈正相关 ( 分别 r=0.557,0.309, 均 P<0.05) 结论 : 肝良恶性肿瘤均可出现肝包膜回缩征, 但两者形态有差异, 与肿瘤大小分化程度及瘤内纤维组织增生程度等密切相关 [ 关键词 ] 肝包膜回缩征 ; 肿瘤 ; 病理 ;CT;MRI Imaging manifestations and pathologic basis for hepatic capsular retraction syndrome caused by benign and malignant liver tumors OU Youkuan 1,2, XIAO Enhua 1, SHANG Quanliang 1, CHEN Juan 1 (1. Department of Radiololgy, Second Xiangya Hospital, Central South University, Changsha ; 2. Department of Radiology, Hospital of Jinjiang City, Jinjiang Fujian , China) ABSTRACT Objective: To investigate the imaging manifestations of CT, MRI and pathological basis for hepatic capsular retraction syndrome caused by benign and malignant liver tumors. Methods: CT or MRI images and pathological features for hepatic capsular retraction syndrome were retrospectively analyzed in 50 patients with benign and malignant liver tumors. Picture archive and communication system (PACS) was used to observe and compare the morphology, size, width, depth, edge of the capsular retraction and the status of liquid under the liver capsule. The structure, differentiation and proliferation of the tumor were analyzed under the microscope. Results: There were malignant liver tumors in 44 patients and benign tumor in 6 patients. The 收稿日期 (Date of reception): 第一作者 (First author): 欧幼宽, @qq.com 通信作者 (Corresponding author): 肖恩华, cjr.xiaoenhua@vip.163.com

福建省晋江市医院影像科, 福建晋江 362200) [ 摘要 ] 目的 : 探讨肝良恶性肿瘤引起包膜回缩征的 CT 和 MRI 表现及其病理基础方法 : 回顾性分析经病理证实的 50 例肝良恶性肿瘤肝包膜回缩征的 CT 和 MRI 表现及病理特点通过影像

2 肝良恶性肿瘤包膜回缩征影像表现及其病理基础欧幼宽, 等 1133 smooth or rough for the edge of capsular retraction was significant difference between the benign tumors and the malignant tumors with three differentiated grades (all P<0.05). There were significant difference in the width and depth for capsule retraction with different amount of fibrous tissues (all P<0.05). The width and depth of capsule retraction were positively correlated to the size of the tumors (r=0.557, respectively, both P<0.05). Conclusion: Benign and malignant hepatic tumors may appear capsule retraction syndrome, but there are morphological differences between them. The differences are closely related with the lesion size, differentiated degree of tumor and fibrous tissue proliferation. KEY WORDS hepatic capsular retraction syndrome; tumor; pathology; CT; MRI 肝包膜回缩征又称肝包膜凹陷征, 是指肝脏包膜平坦或向正常肝轮廓内凹陷 [1], 类似胸膜凹陷 [2-3] 征既往研究多报道肝包膜回缩征为肝恶性肿瘤的特异性征象随着检查设备的不断更新检查的普及, 肝包膜回缩征在肝良性病变亦可观察到本研究回顾性分析 50 例肝良恶性肿瘤患者 CT 和 MRI 包膜回缩征表现并对比病理结果, 比较良恶性肝肿瘤该征象是否存在差异, 以提高对该征象的认识及诊断正确率 1 对象与方法 1.1 对象连续收集中南大学湘雅二医院及晋江市医院 2013 年 7 月至 2015 年 2 月影像及病理资料完整的存在肝包膜回缩征肝肿瘤患者 50 例, 男 35 例, 女 15 例, 年龄 8~77 岁, 病程 1 d~30 余年, 主要症状为腹痛腹胀黄疸乏力纳差等 1.2 检查方法中南大学湘雅二医院患者 44 例,CT 检查采用西门子 (Siemens Somatom Sensation)64 CT 机平扫加 3 期增强扫描, 层厚及层距为 3 和 5 mm, 扫描条件 :120 kv, 150 ma, 先平扫, 后静脉团注造影剂 ( 碘海醇 ), 剂量 1.5 ml/kg 体质量 ; MRI 检查采用飞利浦 (Philips) 公司的 Achieva3.0T X-series 磁共振成像系统横断位脂肪抑制呼吸触发快速自旋回波序列 (turbo spin echo, TSE)T2WI: 重复时间 (repetition time, TR)/ 回波时间 (echo time, TE)=1 277 ms/70 ms, 冠状位 TR/TE=1 647 ms/70 ms, 层厚 / 间距 = 7 mm/1 mm, 视野 (field of view,fov)=370 mm 370 mm, 矩阵 , 信号平均 2 次, 翻转角 90 ; 同反相位横断位呼吸触发快速梯度场回波 (turbo field echo, TFE) T1WI: 同相位 T1-TFE TR/TE =10 ms/2.3 ms, 翻转角 15, 信号平均 2 次, 反相位 T1-TFE TR/TE=10 ms/3.45 ms, 翻转角 15, 信号平均 2 次 ; 动态增强采用 4 期屏气容积扫描 (TR/TE=3.0 ms/1.4 ms), 翻转角 10, 层厚 1 mm, 层间距 0 mm, 先进行平扫, 动脉期扫描延迟时间约 22~25 s, 动脉期扫描后延迟 5 s 开始门静脉期扫描, 门脉期后 4 min 进行延迟扫描, 扫描范围包括全部肝对比剂注射采用 MEDRAD 双筒高压注射器, 注射钆喷酸葡萄甲胺盐 (gadolinium- diethylenetriaminepentaacetate,gd- DTPA) 0.1 mmol/kg, 速率 1.5 ml/s, 后使用 20 ml 生理盐水助推晋江市医院患者 6 例,CT 检查采用 GE16 排螺旋 CT 进行 3 期扫描, 层厚及层距为 10 mm,120 kv,250 ma, 造影剂为碘帕醇, 剂量 1.5 ml/kg; 动脉期扫描 25~30 s, 门脉期扫描 50 s, 延迟期扫描 5 min 扫描范围包括全部肝 1.3 数据测量肝包膜回缩征宽度和深度测量方法如图 1 多发肝包膜回缩征者, 取最大者测量, 将肝包膜回缩的宽度 (W) 分为三个等级 :W 2 cm, 2 cm<w 4 cm,w>4 cm; 回缩深度 (D) 亦分为三个等级 :D 0.5 cm,0.5 cm<d 1 cm,d>1 cm, 观察回缩边缘光整或毛糙有无积液, 由两名影像科主治以上医师通过影像归档和通信系统 (picture archiving and communication systems, PACS) 观察测量并记录

557, 0.309 respectively, both P<0.05). Conclusion: Benign and malignant hepatic tumors may appear capsule retraction syndrome, but there are morphological differences between them.

3 1134 中南大学学报 ( 医学版 ), 2015, 40(10) 2 结果 2.1 病变类型 50 例患者肿瘤均位于肝包膜下, 其中恶性肿瘤 44 例, 良性肿瘤 6 例包括肝细胞癌 20 例, 胆管细胞癌及肝腺癌各 9 例, 转移癌 3 例, 淋巴瘤恶性纤维组织细胞瘤肝母细胞瘤各 1 例, 肝海绵状血管瘤 5 例, 肝血管平滑肌脂肪瘤 1 例图 1 肝包膜回缩测量方法 Figure 1 Measurement method of capsular retraction The red line is the arc edge of the liver capsule, and the black line is the width, and the blue line is the depth 1.4 病理学分析手术标本大体病理与显微病理由两名资深病理医师完成纤维镜下分析病灶内纤维化量的标准如下 : 无纤维化,<25% 对应少量,25%~50% 对应中等量,>50% 对应多量 1.5 统计学处理采用 SPSS11.5 统计学软件行多个独立样本比较的秩和检验及多元相关分析,P<0.05 为差异有统计学意义 2.2 肝包膜回缩征 CT 及 MRI 表现本组良恶性肿瘤肝包膜回缩征宽度深度差异无统计学意义 ( 均 P>0.05) 44 例肝恶性肿瘤分别为 7 种不同细胞类型, 不同类型恶性肿瘤肝包膜回缩情况差异无明显统计学意义 ( 均 P>0.05) 44 例恶性肿瘤中 38 例病理提供了分化程度分析, 良性肿瘤与高中低三个不同分化程度的恶性肿瘤肝包膜回缩征边缘光整或毛糙差异有统计学意义 ( 均 P<0.01, 表 1), 分化程度差的恶性肿瘤肝包膜回缩征边缘毛糙概率明显比高分化肿瘤及良性肿瘤大 ( 图 2) 2.3 病理改变由两位资深病理学家观察分析肿瘤结构内部纤维化量纤维组织量的不同会导致肝包膜回缩宽度深度有差异 ( 均 P<0.05, 表 2) 肿瘤瘤体直径与肝包膜回缩宽度及深度呈正相关 ( 分别 r=0.557,0.309, 均 P<0.05; 表 3) 表 1 良恶性肿瘤肝包膜回缩情况 Table 1 Hepatic capsular retraction of benign and malignant tumors 肿瘤类型 W/ 例 D/ 例边缘情况 / 例是否积液 / 例 W 2 cm 2 cm<w 4 cm W>4 cm D 0.5 cm 0.5 cm<d 1 cm D>1 cm 光整毛糙有无良性高分化中分化低分化总例数 P >0.05 >0.05 <0.01 >0.05 W: 包膜回缩宽度 ;D: 包膜回缩深度总例数

1 例图 1 肝包膜回缩测量方法 Figure 1 Measurement method of capsular retraction The red line is the arc edge of the liver capsule, and the black line is the width, and the blue line is the depth 1.

4 肝良恶性肿瘤包膜回缩征影像表现及其病理基础欧幼宽, 等 1135 A B C D 图 2 良恶性肿瘤肝包膜回缩征 Figure 2 Hepatic capsular retraction of benign and malignant tumors A: Somatom Sensation Siemens 64 CT enhanced coronal reconstruction of portal vein. The edge of capsular retraction is smooth, there is no effusion in the high differentiated hepatocellular carcinoma; B: Somatom Sensation Siemens 64 CT axial enhanced arterial phase. The edge of capsular retraction is rough, no effusion in the differentiation of hepatocellular carcinoma; C: Philips3.0 T magnetic resonance axis TSE T2WI. The edge of capsular retraction is rough, there is small amount of effusion in the poor differentiated hepatocellular carcinoma; D: GE16 CT enhanced arterial phase. The edge of capsular retraction is smooth, there is no effusion in the hepatic hemangioma 表 2 纤维组织量不同肝包膜回缩征差异 Table 2 Different capsular retraction in the different fibrous tissues 纤维化量 W/ 例 D/ 例边缘情况 / 例是否积液 / 例总例数 W 2 cm 2 cm<w 4 cm W>4 cm D 0.5 cm 0.5 cm<d 1 cm D>1 cm 光整毛糙有无无少中多总例数 P <0.05 <0.05 >0.05 >0.05 W: 包膜回缩宽度 ;D: 包膜回缩深度

The edge of capsular retraction is smooth, there is no effusion in the high differentiated hepatocellular carcinoma; B: Somatom Sensation Siemens 64 CT axial enhanced arterial phase.

5 1136 中南大学学报 ( 医学版 ), 2015, 40(10) 表 3 良恶性肿瘤分化等级肿瘤直径纤维增生量与肝包膜回缩征相关分析 Table 3 Correlation analysis of differentiation grade, tumor diameter, fiber hyperplasia and hepatic capsular retraction in the benign and malignant tumors 影像特征良恶性分化等级肿瘤直径纤维量回缩宽度 r P >0.05 >0.05 <0.01 >0.05 回缩深度 r P >0.05 >0.05 >0.05 >0.05 光整 / 毛糙 r P >0.05 <0.01 <0.05 >0.05 积液 r P >0.05 >0.05 <0.05 > 讨论对肝包膜回缩征在恶性肿瘤中报道较多, [4] 良性肿瘤却较少提及 Da Ines 等提出肝包膜回缩是局限性的肝损伤, 但是非特异性的 Blachar [5] 等提出肝包膜回缩征可由局灶性及弥漫性病变引起, 引起因素有肿瘤及非肿瘤病变肿瘤包括原发继发性恶性肿瘤和不典型肝血管瘤的治疗前后, 尤其是某些瘤内含有或可诱导产生大量纤维组织的转移瘤, 如肺癌乳腺癌结肠癌等邻近肝表面的恶性肿瘤侵犯肝窦小血管及小胆管, 形成胆汁淤积性肝硬化, 局部肝萎缩后牵拉包膜形成凹陷 [6] 肿瘤内部中心坏死, 增生的纤维组织牵拉附近的肝包膜使其变平退缩, 甚至呈反弓状或脐凹状, 侵犯肝包膜时呈锯齿状改变 [7-8] 海绵状血管瘤的肝包膜回缩征与瘤内纤维化肿瘤血管血栓栓塞缺血形成有关 [9-10] 非肿瘤因素有肝硬化肝纤维化胆管炎胆管坏死及肝损伤 [11] 肝炎后肝硬化引起的肝包膜凹陷是由肝再生结节及纤维组织增生使肝表面凹凸不平而形成 [12] 随着肝纤维化的进展, 肝包膜回缩程度越明显 [13] 本组病例分别证实了肝包膜回缩征与上述因素有关, 同一患者可多种因素并存亦证实了纤维组织量的不同, 肝包膜回缩征的宽度及深度存在差异笔者认为肝包膜回缩征的因素主要包括以下几个方面 :1) 邻近肝表面的病变内部的炎症坏死轮廓塌陷的负占位效应导致肝包膜回缩 ;2) 病变内部及周围的纤维组织增生牵拉致肝包膜凹陷 ;3) 肿瘤或肿瘤样病变结石炎性病变等阻塞胆管导致胆汁淤积性肝硬化弥漫性肝炎后肝硬化, 肝萎缩后牵拉肝包膜回缩 [14] Fennessy 等报道肝包膜回缩征与转移瘤大小有关, 存在此征者瘤体较大, 这与本研究结果相符, 本组患者肝包膜回缩宽度及深度与肿瘤直径呈正相关, 考虑不仅转移瘤, 其他类型肿瘤肝包膜回缩征大小也可能与肿瘤大小有关, 大瘤体出现肝包膜回缩征的概率明显高于小瘤体, 且随着瘤体增大, 宽度及深度增大 [15] 有研究报道肝包膜回缩征是肝内胆管细胞癌极其重要的间接征象肝包膜回缩征在肿块型肝内胆管细胞癌及低分化肝细胞癌间无明显差异 [16] 本研究结果发现良恶性肿瘤均出现此征, 7 种不同细胞类型恶性肿瘤肝包膜回缩情况无明显差异, 良性肿瘤与高中低三个不同分化等级的恶性肿瘤回缩边缘光整或毛糙差异有统计学意义, 恶性肿瘤分化程度越差, 肝包膜回缩边缘毛糙出现概率越大本组 50 例病变均位于包膜下,17 例患者病理提示肿瘤侵犯肝包膜均为中低分化恶性肿瘤,16 例回缩边缘毛糙曾蒙苏 [17] 等提出当肝包膜回缩征为不规则型时可能提示肿瘤向腹腔内种植或转移笔者认为在排除肝包膜附近的炎性病变后, 肝包膜回缩征边缘毛糙者倾向肿瘤分化程度差, 且存在浸润被膜或腹腔转移的可能对于不同肝包膜回缩征大小形态是否能鉴别恶性程度高低, 还有待进一步证实肝包膜回缩征在肿瘤性病变中以恶性多见, 但并不是特异征象, 良性肿瘤及多种非肿瘤性病变亦可发生良性肿瘤与不同分化程度的恶性肿瘤肝包膜回缩边缘光整或毛糙存在差异, 恶性肿

benign and malignant tumors 影像特征良恶性分化等级肿瘤直径纤维量回缩宽度 r 0.019 0.162 0.557 0.080 P >0.05 >0.05 <0.01 >0.05 回缩深度 r 0.099 0.012 0.309 0.118 P >0.05 >0.05 >0.05 >0.05 光整 / 毛糙 r 0.

6 肝良恶性肿瘤包膜回缩征影像表现及其病理基础欧幼宽, 等 1137 瘤肝包膜回缩边缘毛糙高度提示肿瘤侵犯被膜, 且倾向分化差可能性大肿瘤纤维组织增生量不同肝包膜回缩宽度及深度不同因此, 认真观察此征象, 可初步判断病变良恶性是否侵犯肝被膜肝纤维化程度, 对肿瘤临床分期治疗方案的制定及预后评估有很大帮助, 但仅观察此征是不够的, 还需全面结合病变整体影像表现才能做出完整的诊断参考文献 [1] Blachar A, Federle MP, Sosna J. Liver lesions with hepatic capsular retraction[ J]. Semin Ultrasound CT, 2009, 30(5): [2] Sans N, Fajadet P, Galy-Fourcade D, et al. Is capsular retraction a specific CT sign of malignant liver tumor?[ J]. Eur Radiol, 1999, 9(8): [3] Soyer P, Bluemke DA, Vissuzaine C, et al. CT of hepatic tumors: prevalence and specificity of retraction of the adjacent liver capsule[ J]. Am J Roentgenol, 1994, 162(5): [4] Da Ines D, Petitcolin V, Lannareix V, et al. Liver capsule retraction adjacent to a circumscribed liver lesion: review of 26 cases with histological confirmation[ J]. J Radiol, 2009, 90(9): [5] Blachar A, Federle MP, Brancatelli G. Hepatic capsular retraction: spectrum of benign and malignant etiologies[ J]. Abdom Imaging, 2002, 27(6): [6] 陈星, 王平, 钱林清, 等. 邻表面肝脏病变包膜凹陷 CT 表现及评价 [ J]. 现代医用影像学, 2014, 23(1): CHEN Xing, WANG Ping, QIAN Linqing, et al. The CT manifestation and diagnostic value of liver capsule depressed in diseases adjacent liver surface[ J]. Modern Medical Imageology, 2014, 23(1): [7] 霍福涛. 恶性肝肿瘤邻近肝包膜退缩征的 CT 表现及其评价 [ J]. 中国医学影像技术, 2000, 16(4): HUO Futao. The CT manifestation and diagnostic value of capsular retraction in malignant hepatic tumors[ J]. Chinese Journal of Medical Imaging Technology, 2000, 16(4): [8] 黄可祥, 兰庆茂, 吕亚萍, 等. 肝内胆管细胞癌的多层螺旋 CT 征象分析 [ J]. 中国卫生产业, 2013, 22(8): HUANG Kexiang, LAN Qingmao, LV Yaping, et al. The multi-slice spiral CT imaging signs of intrahepatic cholangiocarcinoma[ J]. China Health Industry, 2013, 22(8): [9] Lim PS, Nazarian LN, Wechsler RJ, et al. Hepatic capsular retraction secondary to involuting cavernous hemangioma[ J]. J Comput Assist Tomogr, 2001, 25(2): [10] Lee SH, Park CM, Cheong IJ, et al. Hepatic capsular retraction: unusual finding of cavernous hemangioma[ J]. J Comput Assist Tomogr, 2001, 25(2): [11] Yang DM, Kim HS, Cho SW, et al. Pictorial review: various causes of hepatic capsular retraction: CT and MR findings[ J]. Br J Radiol, 2002, 75(900): [12] 徐剑峰. 原发性肝细胞癌邻表面肝包膜凹陷 CT 观察及评价 [ J]. 中国交通医学杂志, 2005, 19(6): 701. XU Jianfeng. The CT observation and evaluation of capsular retraction in hepatocellular carcinoma[ J]. Chinese Medical Journal of Communications, 2005, 19(6): 701. [13] Brancatelli G, Baron RL, Federle MP, et al. Focal confluent fibrosis in cirrhotic liver: natural history studied with serial CT[ J]. Am J Roentgenol, 2009, 192(5): [14] Fennessy FM, Mortele KJ, Kluckert T, et al. Hepatic capsular retraction in metastatic carcinoma of the breast occurring with increase or decrease in size of subjacent metastasis[ J]. Am J Roentgenol, 2004, 182(3): [15] 朱昆喜, 洪汛宁. 16 排螺旋 CT 在周围型胆管细胞癌诊断中的应用 [ J]. 江苏医药, 2013, 39(1): ZHU Kunxi, HONG Xunning. Application of spiral 16 slice CT in the diagnosis of peripheral cholangiocarcinoma[ J]. Jiangsu Medical Journal, 2013, 39(1): [16] 赵一珺, 郑丽荣, 杨帆, 等. 肿块型肝内胆管细胞癌与低分化肝细胞癌 CT 影像学特征分析 [ J]. 中国普外基础与临床杂志, 2015, 22(5): ZHAO Yijun, ZHENG Lirong, YANG Fan, et al. CT image features of mass-forming intrahepatic cholangiocarcinoma and poorly differentiated hepatocellular carcinoma[ J]. Chinese Journal of Bases and Clinics in General Surgery, 2015, 22(5): [17] 曾蒙苏, 周康荣. 肝包膜凹陷征在肝癌 CT 诊断中的意义 [ J]. 实用放射学杂志, 1996, 12(6): ZENG Mengsu, ZHOU Kangrong. Clinical value of retraction of the liver capsule in CT diagnosis of hepatocellular carcinoma[ J]. Journal of Practical Radiology, 1996, 12(6): ( 本文编辑傅希文 ) 本文引用 : 欧幼宽, 肖恩华, 尚全良, 陈娟. 肝良恶性肿瘤包膜回缩征影像表现及其病理基础 [ J]. 中南大学学报 : 医学版, 2015, 40(10): DOI: /j.issn Cite this article as: OU Youkuan, XIAO Enhua, SHANG Quanliang, CHEN Juan. Imaging manifestations and pathologic basis for hepatic capsular retraction syndrome caused by benign and malignant liver tumors[ J]. Journal of Central South University. Medical Science, 2015, 40(10): DOI: /j.issn

Liver lesions with hepatic capsular retraction[ J]. Semin Ultrasound CT, 2009, 30(5): 426-435. [2] Sans N, Fajadet P, Galy-Fourcade D, et al.

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