Objective: To analyze the hepatobiliary phase (HBP) image manifestation classification and pathological features of nodules in nodules accompanied by hepatocellular carcinoma (NIN-HCC). Methods: Twenty-five cases cases (27 lesions) with cirrhosis who were confirmed as NIN-HCC by surgical pathology and underwent gadoxetate disodium-enhanced MRI examination before surgery at Nantong Third Hospital affiliated with Nantong University from July 2015 to November 2022 were retrospectively enrolled. The size, signal intensity, enhancement pattern, and pathological features of internal and external nodules were analyzed in NIN-HCC. The lesions score were recorded according to the 2018 version of the Liver Imaging Reporting and Data Systems (LI-RADS) classification criteria. NIN-HCCs were grouped and typed according to the different HBP signal intensities of the inner and outer nodules. The independent-samples t-test, Mann-Whitney U test or Fisher's exact probability method were used to compare the differences in imaging features and LI-RADS scores between the groups. The Spearman correlation coefficient was used to evaluate the correlation between the pathological differentiation degree of internal and external nodules and the HBP signal intensity. The Kaplan-Meier curve was used to analyze recurrence-free survival (RFS) following NIN-HCC surgery. Results: The internal nodules of the 27 NIN-HCCs showed altered hypervascularity with a maximum diameter of (13.2±5.5) mm during the arterial phase. 51.9% (14/27) and 48.1% (13/27) showed "fast in and fast out" and fast in and slow out"enhancement patterns. The external nodules showed altered hypovascularity with a maximum diameter of (25.7±7.3) mm, and 13 (48.1%) of them were accompanied to manifest during the arterial phase. NIN-HCC was divided into two groups according to the signal intensity of HBP of the outer nodules with the background liver parenchyma signal intensity as a reference: the hyposignal group (n=17, 63.0%) and the isosignal group (n=10, 37.0%). The hyposignal group and the isosignal group were divided into A~C type and D~F type, a total of six types, according to the hypo, iso, and hyper signals of the inner nodules and the signal intensity of the outer nodules as a reference. Within the hyposignal group, 7.4% (2/27) of the inner nodules showed hyposignal (type A), 37.0% (10/27) showed isosignal (type B), and 18.5% (5/27) showed hypersignal (type C). Within the isosignal group, 29.6% (8/27) of the inner nodules showed hyposignal (type D), 7.4% (2/27) showed isosignal (type E), and there was no hypersignal (type F). 40.7% (11/27) of the lesions were LR-4 in LI-RADS score, and 59.3% (16/27) were LR-5. There was no statistically significant difference (P>0.05) in the maximum diameter, enhancement pattern, and LI-RADS score of internal and external nodules between the hypo and iso signal group. Histologically, NIN-HCC showed fine trabecular/pseudoglandular duct type without microvascular invasion, among which the inner nodules were mainly moderately differentiated HCC, and the outer nodules were mainly well-differentiated HCC. The degree of differentiation between the inner and outer nodules and the HBP signal intensity had no statistically significant difference (r=0.290, P=0.143; r=0.079, P=0.697). The median RFS follow-up time after NIN-HCC radical resection was 31.7 months, and the cumulative RFS rates at 1, 3, and 5 years were 96.0%, 76.0%, and 64.0%, respectively. Conclusions: NIN-HCC can serve as a morphological marker for early-stage diagnosis of multi-step cancer evolution in HCC, with certain imaging and pathological features. HBP imaging classification is helpful to enhance the diagnostic recognition of this disease.
目的： 分析肝细胞癌伴“结中结”（NIN-HCC）的肝胆期（HBP）影像表现分型及其病理学特征。 方法： 回顾性连续纳入2015年7月至2022年11月于南通大学附属南通第三医院经手术病理证实为NIN-HCC，术前进行过钆塞酸二钠增强MRI检查的25例（27个病灶）肝硬化患者。分析并记录NIN-HCC中内、外结节的大小、信号强度、强化方式及其病理学特征，并根据2018版肝脏影像报告与数据系统（LI-RADS）分类标准对病灶进行评分。根据内、外结节的HBP不同信号强度，将NIN-HCC进行分组、分型。采用独立样本t检验、Mann-Whitney U检验或Fisher确切概率法比较组间的影像特征及LI-RADS评分的差异。采用Spearman相关系数评估内、外结节的病理分化程度与HBP信号强度之间的相关性。采用Kaplan-Meier曲线分析NIN-HCC术后无复发生存（RFS）。 结果： 27个NIN-HCC中，内结节动脉期均呈富血供改变，最大径（13.2±5.5）mm，51.9%（14/27）呈“快进快出”强化，48.1%（13/27）呈“快进慢出”强化。外结节动脉期均呈乏血供改变，最大径（25.7±7.3）mm，13个（48.1%）伴廓清表现。以背景肝实质信号强度作为参照，根据外结节HBP的信号强度，将NIN-HCC分为2组：低信号组（n=17，63.0%）及等信号组（n=10，37.0%）。以外结节信号强度作为参照，根据内结节低、等、高信号，将低信号组、等信号组依次分为A～C型、D～F型，共6型。低信号组中，7.4%（2/27）内结节呈更低信号（A型），37.0%（10/27）呈等信号（B型），18.5%（5/27）呈高信号（C型）。等信号组中，29.6%（8/27）内结节呈低信号（D型），7.4%（2/27）呈等信号（E型），无一例高信号（F型）。40.7%（11/27）病灶LI-RADS评分为LR-4类，59.3%（16/27）为LR-5类。低信号组与等信号组间，内、外结节最大径、强化方式及病灶LI-RADS评分差异均无统计学意义（P值均＞0.05）。组织学上，NIN-HCC呈细梁/假腺管型，无微血管侵犯，其中内结节以中分化HCC为主，外结节以高分化HCC为主。内、外结节的分化程度与HBP信号强度差异无统计学意义（r=0.290，P=0.143；r=0.079，P=0.697）。NIN-HCC根治性切除术后中位RFS随访时间为31.7个月，1、3、5年累积RFS率分别为96.0%、76.0%和64.0%。 结论： NIN-HCC可作为HCC多步癌演变早期诊断的形态学标志物，影像及病理学具有一定特征性，HBP影像学分型有助于进一步提高HCC伴“结中结”影像征象的了解。.