Abstract
目的
比较肾透明细胞癌与非透明细胞癌伴静脉癌栓患者的临床病理特征及预后。
方法
连续性纳入2014年1月至2024年2月北京大学第三医院泌尿外科收治的肾细胞癌伴静脉癌栓患者的临床和病理资料进行回顾性分析, 根据病理类型分为透明细胞癌组和非透明细胞癌组, 比较两组患者基线、术中和预后情况。采用Kaplan-Meier方法绘制生存曲线。
结果
共纳入437例患者, 中位年龄58岁, 男性317例, 女性120例, 透明细胞癌组366例, 非透明细胞癌组71例。非透明细胞癌组包括乳头状肾细胞癌38例(53.5%)、嫌色细胞肾细胞癌2例(2.8%)、未分类肾细胞癌11例(15.5%)、分子定义的肾细胞癌19例(26.8%)和肾集合管癌1例(1.4%)。相较于肾透明细胞癌组, 非透明细胞癌组患者发病年龄较早(59岁vs. 55岁, P=0.010), 肿瘤直径更大(8.4 cm vs. 9.5 cm, P=0.025)、淋巴结转移比例较高(56.8% vs. 70.6%, P=0.034)、癌栓分级(P < 0.001)和病理分级较晚(P=0.010)、手术时间较长(272 min vs. 289 min, P=0.023)、总生存期较短(80个月vs. 35个月, P < 0.001)。多因素Cox分析显示与肾细胞癌伴静脉癌栓患者预后相关的因素为病理类型、远处转移、癌栓分级、肉瘤样或横纹肌样分化。两组在性别、体重指数、肿瘤侧别、远处转移、肉瘤样或横纹肌样分化、美国麻醉医师协会评分、手术方式选择、转为开放手术比例、失血量、输注红细胞、输注血浆等方面差异均无统计学意义。
结论
相较于肾透明细胞癌伴静脉癌栓患者, 非透明细胞癌伴静脉癌栓患者发病年龄早、疾病侵袭性强、预后差。
Keywords: 肾细胞癌, 静脉癌栓, 回顾性, 预后
Abstract
Objective
To compare the clinicopathological characteristics and prognostic outcomes between patients with clear cell renal cell carcinoma (ccRCC) and non-clear cell renal cell carcinoma (nccRCC) accompanied by venous tumor thrombus.
Methods
A retrospective analysis was conducted on clinical and pathological data from patients with RCC and venous tumor thrombus treated in the Department of Urology at Peking University Third Hospital between January 2014 and February 2024. Patients were stratified into two groups based on pathological type: ccRCC and nccRCC. Comparisons of baseline characteristics, intraoperative situation, and prognosis between the two groups were performed using t-tests, Mann-Whitney U tests, chi-square tests, and Log-rank tests. Survival curves were generated using the Kaplan-Meier method.
Results
A total of 437 patients were included, with a median age of 58 years, including 317 males and 120 females. The cohort comprised 366 cases of ccRCC and 71 cases of nccRCC. The non-clear cell group included 38 cases (53.5%) of papillary renal cell carcinoma, 2 cases (2.8%) of chromophobe renal cell carcinoma, 11 cases (15.5%) of unclassified renal cell carcinoma, 19 cases (26.8%) of molecularly defined renal cell carcinoma, and 1 case (1.4%) of collecting duct carcinoma. Compared with the clear cell renal carcinoma group, patients in the non-clear cell carcinoma group demonstrated a younger age at diagnosis (59 years vs. 55 years, P=0.010), larger tumor size (8.4 cm vs. 9.5 cm, P=0.025), higher rates of lymph node metastasis (56.8% vs. 70.6%, P=0.034), more advanced tumor thrombus (P < 0.001) and pathological grading (P=0.010), longer surgical duration (272 minutes vs. 289 minutes, P=0.023), and shorter overall survival (80 months vs. 35 months, P < 0.001). Multivariate Cox analysis indicated that histologic type, distant metastasis, tumor thrombus grading, and sarcomatoid/rhabdoid differentiation were prognostic factors in the renal cell carcinoma patients with venous tumor thrombus. No significant differences were observed between the two groups in terms of gender, body mass index, tumor laterality, distant metastasis, sarcomatoid or rhabdoid differentiation, American Society of Anesthesiologists (ASA) score, surgical approach, conversion to open surgery, blood loss, or transfusion of red blood cells and plasma.
Conclusion
Compared with patients with clear cell renal carcinoma and venous tumor thrombus, those with non-clear cell carcinoma and venous tumor thrombus exhibit earlier onset, more aggressive disease progression, and poorer prognosis.
Keywords: Renal cell carcinoma, Venous tumor thrombus, Retrospective, Prognosis
肾细胞癌(renal cell carcinoma, RCC)是泌尿系统最常见的恶性肿瘤之一, 2022年我国新发病例约7.3万例, 死亡人数约2.4万例[1]。侵袭性肾细胞癌具有症状隐匿的特点, 4% ~10%的患者会发展为合并肾静脉或下腔静脉癌栓[2]。肾细胞癌伴静脉癌栓患者如不采取积极治疗措施, 总生存期(overall survival, OS)仅为5个月, 1年肿瘤特异生存率(cancer specific survival, CSS)仅为29%[3]。根治性肾切除术+静脉癌栓取出术可以显著改善肾细胞癌合并癌栓患者预后, 非转移性患者术后5年CSS为34.0%~71.0%[4]。肾透明细胞癌(clear cell renal cell carcinoma, ccRCC)是最常见的RCC组织类型, 占RCC全部病例的75%[5]。既往有研究报道相较于ccRCC患者, 乳头状RCC伴癌栓患者的淋巴结转移概率更高, 且CSS更低[6-7]。全面评估ccRCC与非透明肾细胞癌(non-clear cell renal cell carcinoma, nccRCC)患者伴静脉癌栓患者临床病理信息与预后比较的研究非常匮乏。美国约翰霍普金斯大学团队的一项研究结果表明, 除病理N分期外, ccRCC与nccRCC组间在所有基线数据和OS等方面差异均无统计学意义[8]。13家欧洲单位联合开展的另一项研究结果同样显示病理学类型对肾细胞癌伴下腔静脉癌栓患者OS无显著影响[9]。本课题组既往开展的一项针对青年肾细胞癌伴瘤栓患者研究结果显示, nccRCC的术后复发率和死亡率更高[10]。本研究旨在比较ccRCC与nccRCC伴静脉癌栓患者的临床病理特征、围手术期各项指标及预后, 为临床实践提供参考。
1. 资料与方法
1.1. 病例选择
连续性纳入2014年1月至2024年2月北京大学第三医院泌尿外科收治的肾细胞癌伴静脉癌栓患者的临床和病理资料进行回顾性分析。纳入标准: (1)年龄≥ 18岁；(2)接受根治性肾切除术和癌栓取出术治疗；(3)术后组织病理学信息确诊为肾细胞癌；(4)病历资料(包括年龄、性别、手术方式等)信息齐全；(5)术后随访信息完整。排除标准: (1)存在严重心肺功能不全、凝血功能异常等相对手术禁忌证或麻醉禁忌证者；(2)临床重要信息缺失者。采用Mayo分级标准对癌栓进行分级评估[11], 根据美国麻醉医师协会(American Society of Anesthe-siologists, ASA)分级标准评估患者术前全身状态, 组织学类型按照2022年世界卫生组织(World Health Organization, WHO)肾脏肿瘤分类标准[12]。本研究开始前已经北京大学第三医院医学伦理委员会审查批准(S2024708)。
1.2. 术后随访
对患者进行术后随访, 随访内容为患者的生存信息, 主要观察终点为全因死亡, 定义为各种原因发生的死亡事件。OS定义为手术日期至全因死亡或末次随访的时间。
1.3. 统计学分析
应用GraphPad Prism 8软件, 对于计量资料, 若符合正态性分布, 采用均数±标准差表示, 两组间比较采用独立样本t检验；若计量资料不符合正态性分布, 使用中位数(四分位间距)表示, 两组间比较采用Mann-Whitney U秩和检验。对于计数资料, 采用n(%)表示, 若为无序分类资料, 采用卡方检验；若为有序分类资料, 采用Mann-Whitney U秩和检验。采用Kaplan-Meier方法绘制生存曲线, 采用Log-rank检验对患者的OS进行分析。P < 0.05认为差异有统计学意义。
2. 结果
共纳入437例肾细胞癌伴静脉癌栓患者(表 1), 其中ccRCC组患者366例(83.8%), nccRCC组患者71例(16.2%)。ccRCC组患者发病年龄大于nccRCC组(59岁vs. 55岁, P=0.010)。ccRCC组和nccRCC组分别纳入男性270例(73.8%)和47例(66.2%), 女性96例(26.2%)和24例(33.8%), 组间差异无统计学意义(P=0.191)。两组患者体重指数(body mass index, BMI)分别为24.0和24.1 kg/m2, 组间差异无统计学意义(P=0.734)。两组患者肿瘤侧别分别为左侧135例vs. 32例、右侧231例vs. 39例, 差异无统计学意义(P=0.194)。nccRCC组患者的病理类型分别为乳头状肾细胞癌38例(53.5%)、嫌色细胞肾细胞癌2例(2.8%)、未分类肾细胞癌11例(15.5%)、分子定义的肾细胞癌19例(26.8%)和肾集合管癌1例(1.4%)。在肿瘤直径方面, ccRCC组显著小于nccRCC组(8.4 cm vs. 9.5 cm, P=0.025)。ccRCC组淋巴结转移率少于nccRCC组(56.8% vs. 70.6%, P=0.034), 而两组在远处转移方面差异无统计学意义(26.2% vs. 37.6%, P=0.074)。ccRCC组和nccRCC组患者的癌栓分级分布分别为0级(26.5% vs. 21.1%)、1级(16.7% vs. 16.9%)、2级(42.1% vs. 39.4%)、3级(6.8% vs. 16.9%)和4级(7.9% vs. 5.7%), 差异有统计学意义(P < 0.001)。在肉瘤样或横纹肌样分化方面, ccRCC组和nccRCC组比例分别为15.6%和8.5%, 差异无统计学意义(P=0.118)。在病理学分级方面, ccRCC组的3~4级比例明显少于nccRCC组比例(61.5% vs. 77.5%), 差异有统计学意义(P=0.010)。两组在ASA分级方面差异无统计学意义(P=0.233)。
表 1.
肾透明细胞癌与非透明细胞癌伴静脉癌栓患者的临床病理特征比较
Baseline clinical and tumor characteristics of clear cell and non-clear cell renal cell carcinoma patients with venous tumor thrombus
| Variables | Total | ccRCC | nccRCC | P |
| Data were M (IQR). BMI, body mass index; IQR, interquartile range; ccRCC, clear cell renal cell carcinoma; nccRCC, non-clear cell renal cell carcinoma; ASA, American Society of Anesthesiologists. | ||||
| Number of patients | 437 (100.0) | 366 (83.8) | 71 (16.2) | |
| Age/years | 58 (14) | 59 (8) | 55 (18) | 0.010 |
| Gender | 0.191 | |||
| Male | 317 (72.5) | 270 (73.8) | 47 (66.2) | |
| Female | 120 (27.5) | 96 (26.2) | 24 (33.8) | |
| BMI/(kg/m2) | 24.0 (4.7) | 24.0 (5.0) | 24.1 (4.1) | 0.734 |
| Tumor laterality | 0.194 | |||
| Left | 167 (38.2) | 135 (36.9) | 32 (45.1) | |
| Right | 270 (61.8) | 231 (63.1) | 39 (54.9) | |
| Histologic type | ||||
| Clear cell | 366 (83.8) | 366 (100) | - | |
| Papillary | 38 (8.7) | - | 38 (53.5) | |
| Chromophobe | 2 (0.5) | - | 2 (2.8) | |
| Unclassified | 11 (2.5) | - | 11 (15.5) | |
| Molecularly defined | 19 (4.3) | - | 19 (26.8) | |
| Collecting duct | 1 (0.2) | - | 1 (1.4) | |
| Tumor diameter/cm | 8.6 (3.8) | 8.4 (3.9) | 9.5 (4.1) | 0.025 |
| N | 0.034 | |||
| N0 | 177 (40.5) | 158 (43.2) | 20 (29.4) | |
| N1 | 260 (59.5) | 208 (56.8) | 48 (70.6) | |
| M | 0.074 | |||
| M0 | 315 (72.1) | 270 (73.8) | 45 (63.4) | |
| M1 | 122 (27.9) | 96 (26.2) | 26 (37.6) | |
| Tumor thrombus grading | < 0.001 | |||
| 0 | 112 (25.6) | 97 (26.5) | 15 (21.1) | |
| 1 | 73 (16.7) | 61 (16.7) | 12 (16.9) | |
| 2 | 182 (41.6) | 154 (42.1) | 28 (39.4) | |
| 3 | 37 (8.5) | 25 (6.8) | 12 (16.9) | |
| 4 | 33 (7.6) | 29 (7.9) | 4 (5.7) | |
| Sarcomatoid/rhabdoid differentiation | 0.118 | |||
| Absent | 374 (85.6) | 309 (84.4) | 65 (91.5) | |
| Present | 63 (14.4) | 57 (15.6) | 6 (8.5) | |
| Pathologic grade | 0.010 | |||
| 1-2 | 157 (35.9) | 141 (38.5) | 16 (22.5) | |
| 3-4 | 280 (64.1) | 225 (61.5) | 55 (77.5) | |
| ASA grade | 0.233 | |||
| 1-2 | 367 (84.0%) | 304 (83.1) | 63 (88.7) | |
| 3-4 | 70 (16.0) | 62 (16.9) | 8 (11.3) | |
在手术方面(表 2), ccRCC组和nccRCC组的术式选择分别为: 开放手术(33.9% vs. 46.5%)、腹腔镜手术(43.2% vs. 32.4%)和机器人手术(22.9% vs. 21.1%), 差异无统计学意义(P=0.112)。此外, 两组在腹腔镜或机器人手术中转为开放手术的比例方面差异无统计学意义(2.9% vs. 2.6%, P>0.999)。ccRCC组中位手术时间明显少于nccRCC组(272 min vs. 289 min, P=0.023)。ccRCC组和nccRCC组在失血量(500 mL vs. 575 mL, P=0.361)、输注悬浮红细胞(400 mL vs. 0 mL, P=0.316)和输注血小板(0 mL vs. 0 mL, P=0.591)方面差异均无统计学意义。
表 2.
接受根治性肾切除术+静脉癌栓取出术的肾透明细胞癌与非透明细胞癌伴静脉癌栓患者的术中情况比较
Intraoperative situation of clear cell and non-clear cell renal cell carcinoma patients with venous tumor thrombus
| Variables | Total | ccRCC | nccRCC | P |
| Data were M (IQR). * The conversion rate from laparoscopic and robotic surgery to open surgery; IQR, interquartile range; ccRCC, clear cell renal cell carcinoma; nccRCC, non-clear cell renal cell carcinoma. | ||||
| Number of patients | 437 (100.0) | 366 (83.8) | 71 (16.2) | |
| Radical nephrectomy approach | 0.112 | |||
| Open | 157 (35.9) | 124 (33.9) | 33 (46.5) | |
| Laparoscopic | 181 (41.4) | 158 (43.2) | 23 (32.4) | |
| Robotic | 99 (22.7) | 84 (22.9) | 15 (21.1) | |
| Conversion to open surgery* | 8 (2.9) | 7 (2.9) | 1 (2.6) | >0.999 |
| Duration of surgery/min | 273 (171) | 272 (164) | 289 (170) | 0.023 |
| Estimated blood loss/mL | 500 (900) | 500 (900) | 575 (857) | 0.361 |
| RBC transfusion/mL | 400 (800) | 400 (800) | 0 (800) | 0.316 |
| Plasma transfusion/mL | 0 (400) | 0 (400) | 0 (400) | 0.591 |
为进行多因素Cox分析(表 3), 将患者根据年龄分为＜60岁及≥60岁组, 根据BMI分为＜24 kg/m2组和≥24 kg/m2组, 根据肿瘤直径分为＜8.5 cm和≥8.5 cm组。纳入病理类型、性别、发病年龄、BMI、癌栓分级、肿瘤侧别、肿瘤直径、淋巴结转移、远处转移、肉瘤样或横纹肌样分化、病理学分级、ASA分级、手术方式进入单因素Cox分析, 结果有统计学意义的因素有BMI、病理类型、远处转移、癌栓分级、肉瘤样或横纹肌样分化、病理学分级、手术方式。多因素分析发现, 与肾细胞癌伴静脉癌栓患者预后相关的因素为病理类型、远处转移、癌栓分级、肉瘤样或横纹肌样分化。
表 3.
肾细胞癌伴静脉癌栓患者预后相关的Cox回归分析
Prognosis-related Cox regression analysis in patients with renal cell carcinoma patients with venous tumor thrombus
| Variables | Univariate analysis | Multivariate analysis | |||
| HR (95%CI) | P | HR (95%CI) | P | ||
| BMI, body mass index. | |||||
| Age/years | |||||
| < 60 | |||||
| ≥60 | 1.344 (0.981, 1.841) | 0.066 | |||
| Gender | |||||
| Male | |||||
| Female | 0.931 (0.651, 1.332) | 0.695 | |||
| BMI/(kg/m2) | |||||
| < 24 | |||||
| ≥24 | 0.626 (0.456, 0.859) | 0.004 | 0.772 (0.553, 1.078) | 0.128 | |
| Tumor laterality | |||||
| Left | |||||
| Right | 0.921 (0.671, 1.264) | 0.611 | |||
| Histologic type | |||||
| Clear cell | |||||
| Non-clear cell | 2.386 (1.670, 3.409) | < 0.001 | 2.277 (1.561, 3.321) | < 0.001 | |
| Tumor size/cm | |||||
| < 8.5 | |||||
| ≥8.5 | 1.199 (0.879, 1.637) | 0.252 | |||
| N | |||||
| N0 | |||||
| N1 | 1.270 (0.919, 1.756) | 0.148 | |||
| M | |||||
| M0 | |||||
| M1 | 2.582 (1.882, 3.543) | < 0.001 | 2.250 (1.609, 3.146) | < 0.001 | |
| Tumor thrombus grading | |||||
| 0 | |||||
| 1 | 1.102 (0.657, 1.848) | 0.712 | 0.986 (0.584, 1.666) | 0.958 | |
| 2 | 1.246 (0.818, 1.896) | 0.306 | 1.275 (0.824, 1.975) | 0.276 | |
| 3 | 2.082 (1.207, 3.589) | 0.008 | 1.502 (0.816, 2.766) | 0.192 | |
| 4 | 2.399 (1.367, 4.211) | 0.002 | 2.208 (1.207, 4.040) | 0.010 | |
| Sarcomatoid/rhabdoid differentiation | |||||
| Absent | |||||
| Present | 2.168 (1.454, 3.235) | < 0.001 | 2.309 (1.520, 3.509) | < 0.001 | |
| Pathologic grade | |||||
| 1-2 | |||||
| 3-4 | 1.931 (1.362, 2.738) | < 0.001 | 1.432 (0.998, 2.056) | 0.051 | |
| ASA grade | |||||
| 1-2 | |||||
| 3-4 | 1.399 (0.939, 2.083) | 0.098 | |||
| Radical nephrectomy approach | |||||
| Open | |||||
| Laparoscopic | 1.483 (1.067, 2.060) | 0.019 | 0.872 (0.596, 1.276) | 0.481 | |
| Robotic | 0.884 (0.512, 1.525) | 0.657 | 0.614 (0.349, 1.081) | 0.091 | |
在预后方面(图 1), ccRCC组患者OS明显优于nccRCC组, 中位生存时间分别为80个月和35个月, 差异有统计学意义(P < 0.001)。
图 1.
肾透明细胞癌与非透明细胞癌伴静脉癌栓患者总生存期比较
Kaplan-Meier survival curves for clear cell and non-clear cell renal cell carcinoma (ccRCC and nccRCC) patients with venous tumor thrombus compared with overall survival
3. 讨论
肾细胞癌是泌尿外科系统高发的恶性肿瘤, 发病率以每年2%~3%的速度递增[13]。肾细胞癌伴静脉癌栓患者在初诊时一般分期较晚, 身体状况较差, 既往多采取非手术治疗。随着医疗水平和外科设备的不断进步, 患者接受根治性肾切除术和癌栓取出术的成功率显著提高, 肾细胞癌的预后得到极大改善[14]。近年来, 肾细胞癌合并静脉癌栓患者的临床研究已成为肿瘤学领域的重要研究方向, 但绝大多数既往研究只纳入ccRCC患者进行分析。本研究综合比较ccRCC和nccRCC伴静脉癌栓临床病理特征与预后, 发现两组患者在基线特征与OS等方面均存在较大差异, 在临床实践中应引起重视。
既往研究对比较ccRCC和nccRCC伴静脉癌栓的关注相对不足, 一项13家欧洲单位共纳入1 192例肾细胞癌伴下腔静脉癌栓患者, 其中包括1 039例ccRCC、34例乳头状RCC、16例嫌色RCC、14例肾集合管癌、9例其他类型肾细胞癌和80例病理数据缺失患者, 结果显示在多因素分析中病理学类型未显示出对OS的显著影响[9]。另一项在美国开展的多中心研究纳入1 594例ccRCC、151例乳头状RCC、29例嫌色RCC患者, 多因素分析结果显示与ccRCC相比, 乳头状RCC伴静脉癌栓患者的5年CSS更低, 而嫌色RCC患者则没有明显差异[7]。韩国开展的一项比较ccRCC与2型乳头状RCC伴静脉癌栓患者的研究表明2型乳头状RCC的CSS更低[15]。本课题组既往开展的一项研究显示相较于ccRCC伴静脉癌栓患者, 2型乳头状RCC的淋巴转移率更高、CSS更低[6]。然而上述研究未纳入手术时间、估计失血量等因素综合分析。一项约翰霍普金斯大学开展的比较ccRCC与nccRCC伴静脉癌栓患者情况的研究, 纳入82例ccRCC和21例nccRCC患者, 结果显示除病理N分期外, 两组在所有基线数据和OS等方面差异均无统计学意义, 但该研究纳入病例数量相对较少, 结论有待进一步验证。
本研究发现相较于ccRCC, nccRCC伴静脉癌栓的侵袭性更强、治疗难度更大。无论在疾病早期筛查, 亦或是手术方案制定、术后治疗方案制定等各个方面, 针对nccRCC伴静脉癌栓患者均需更加引起重视。既往部分研究与本文结果存在差异, 分析可能原因包括人种差异、既往研究纳入患者数量相对较少、辅助治疗药物不同等。
新辅助治疗联合手术在一系列肾细胞癌伴静脉癌栓的临床研究中展示出良好的疗效, 但大多数研究纳入人群为ccRCC患者。英国开展的一项多中心Ⅱ期临床试验纳入20例ccRCC伴下腔静脉癌栓患者, 75%的患者癌栓长度出现缩减[16]。然而当研究纳入nccRCC患者时结果不容乐观, 美国开展的一项研究纳入19例ccRCC和6例未分类RCC, 结果显示只有1例患者在接受靶向治疗后出现瘤栓回缩[17]。综合上述临床试验结果, nccRCC伴静脉癌栓患者接受以靶向治疗为主的新辅助治疗效果欠佳, 在免疫治疗联合靶向治疗数据较为匮乏。
本研究存在一定局限性: 首先, 本研究为单中心回顾性研究, 研究结果未来需要更大样本量的多中心研究以进一步验证；其次, 本研究部分数据跨度时间长, 且未纳入术后辅助治疗信息。
综上所述, 相较于肾透明细胞癌伴静脉癌栓患者, 非透明细胞癌伴静脉癌栓患者的发病年龄更早、疾病侵袭性更强、预后更差, 临床上对此类患者应制定更具有针对性的治疗方案, 从而有效改善患者预后。
Funding Statement
国家自然科学基金(82473287)和北京市自然科学基金(7232212)
Supported by the National Natural Science Foundation of China (82473287), the Beijing Natural Science Foundation (7232212)
Footnotes
利益冲突 所有作者均声明不存在利益冲突。
作者贡献声明 郭博达、陆敏: 收集、分析、整理数据, 撰写论文；王国良、张洪宪、刘磊、侯小飞: 设计研究方案；赵磊、田晓军: 总体把关和审定论文；张树栋: 提出研究思路, 总体把关和审定论文。
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