伴静脉癌栓的肾上腺皮质癌的临床治疗及预后

doi:10.19723/j.issn.1671-167X.2024.04.013

摘要/Abstract

摘要：

目的: 分析肾上腺皮质癌伴静脉癌栓患者的临床病理特征、预后，并总结手术治疗经验。方法: 回顾性分析北京大学第三医院泌尿外科2018—2023年接受手术治疗的肾上腺皮质癌患者的相关数据，将其分为伴静脉癌栓组和不伴静脉癌栓组。采用Wilcoxon秩和检验比较定量变量，卡方检验/Fisher精确检验比较分类变量，采用Kaplan-Meier法计算生存率。结果: 共纳入27例肾上腺皮质癌患者，其中11例(40.7%)伴静脉癌栓，包括8例女性，3例男性，中位年龄49(36，58)岁，中位体重指数26.0(24.1，30.4) kg/m²；7例初诊时有症状，6例有高血压病史，2例皮质醇水平增高；中位肿瘤直径9.4(6.5，12.5) cm。3例肿瘤侧别为左侧，其中1例局限在左肾上腺中央静脉未侵入左肾静脉，2例癌栓生长达肝下下腔静脉；8例肿瘤侧别为右侧，其中1例在右肾上腺中央静脉未侵入下腔静脉，4例侵入肝下下腔静脉，3例生长达肝后下腔静脉。10例患者为欧洲肾上腺肿瘤研究协作网(European Network for the Study of Adrenal Tumors，ENSAT)临床分期Ⅲ期，1例为Ⅳ期。手术方式为开放手术6例，单纯腹腔镜手术者4例，机器人辅助腹腔镜手术1例；2例切除同侧肾脏；中位手术时间332(261，440) min，术中中位出血量900(700，2 200) mL，术后中位住院时间9(5，10) d；中位生存时间24.0个月，中位复发时间7.0个月，16例不伴静脉癌栓患者均未达到中位生存时间和中位复发时间。与不伴静脉癌栓组相比，静脉癌栓组有更差的3年总体生存(overall survival，OS)率(71.4% vs. 40.9%；Log-rank，P=0.038)和2年无复发生存(recurrence-free survival，RFS)率(53.7% vs. 9.1%；Log-rank，P=0.015)。结论: 肾上腺皮质癌伴静脉癌栓患者预后较差，肾上腺肿瘤切除术和静脉癌栓取出术治疗该疾病安全有效。

关键词: 肾上腺皮质癌, 癌栓, 临床病理特征, 预后

Abstract:

Objective: To analyze the clinicopathological features, prognostic value and surgical treatment experience in patients with adrenocortical carcinoma with venous tumor thrombus. Methods: We collected relevant data of the patients with adrenocortical carcinoma who had undergone surgery in Peking University Third Hospital from 2018 to 2023. The patients were divided into venous tumor thrombus group and non-tumor thrombus group. The Wilcoxon rank sum test was used to compare the quantitative variables. The chi-squared test and Fisher's exact test were used to compare the categorical variables. The Kaplan-Meier method was used to estimate the survival rate. Results: A total of 27 patients with adrenocortical carcinoma were included, of whom 11 cases (40.7%) had venous tumor thrombus. In the patients with venous tumor thrombus, 8 patients were female and 3 were male. The median age was 49 (36, 58) years. The median body mass index was 26.0 (24.1, 30.4) kg/m². Seven patients presented with symptoms at their initial visit. Six patients had a history of hypertension. Elevated levels of cortisol were observed in 2 cases. Three tumors were found on the left side, while 8 were found on the right side. Median tumor diameter was 9.4 (6.5, 12.5) cm. On the left, there was a case of tumor thrombus limited to the central vein of the left adrenal gland without invasion into the left renal vein, and two cases of tumor thrombus growth extending into the inferior vena cava below the liver. One case of tumor thrombus on the right adrenal central vein did not invade the inferior vena cava. Four cases of tumor thrombus invaded the inferior vena cava below the liver and three cases extended to the posterior of the liver. Ten patients were in European Network for the Study of Adrenal Tumors (ENSAT) stage Ⅲ and one was in ENSAT stage Ⅳ. Open surgery was performed in 6 cases, laparoscopic surgery alone in 4 cases and robot-assisted laparoscopic surgery in 1 case. Two patients underwent ipsilateral kidney resection. Median operative time was 332 (261, 440) min. Median intraoperative bleeding was 900 (700, 2 200) mL. Median hospital stay was 9 (5, 10) days. Median survival time for the patients with tumor thrombus was 24.0 months and median time to recurrence was 7.0 months. The median survival and recurrence time of 16 patients without tumor thrombus were not reached. The patients with tumor thrombus had worse 3-year overall survival (OS) rate (40.9% vs. 71.4%; Log-rank, P=0.038) and 2-year recurrence-free survival (RFS) (9.1% vs.53.7%; Log-rank, P=0.015) rates compared with the patients with non-tumor thrombus. Conclusion: Patients with adrenocortical carcinoma with venous tumor thrombus have poor prognosis. Different adrenal tumor resections and venous tumor thrombus removal procedures based on different tumor thrombus locations are safe and effective in treating this disease.

Key words: Adrenocortical carcinoma, Tumor thrombus, Clinicopathological features, Prognosis

中图分类号:

R699.3

刘帅,刘磊,刘茁,张帆,马潞林,田晓军,侯小飞,王国良,赵磊,张树栋. 伴静脉癌栓的肾上腺皮质癌的临床治疗及预后[J]. 北京大学学报（医学版）, 2024, 56(4): 624-630.

Shuai LIU,Lei LIU,Zhuo LIU,Fan ZHANG,Lulin MA,Xiaojun TIAN,Xiaofei HOU,Guoliang WANG,Lei ZHAO,Shudong ZHANG. Clinical treatment and prognosis of adrenocortical carcinoma with venous tumor thrombus[J]. Journal of Peking University (Health Sciences), 2024, 56(4): 624-630.

图/表 4

表1

表2

表3

图1

参考文献 25

1	Calissendorff J , Calissendorff F , Falhammar H . Adrenocortical cancer: Mortality, hormone secretion, proliferation and urine ste-roids: Experience from a single centre spanning three decades[J]. BMC Endocr Disord, 2016, 16, 15. doi: 10.1186/s12902-016-0095-9
2	De Filpo G , Mannelli M , Canu L . Adrenocortical carcinoma: Current treatment options[J]. Curr Opin Oncol, 2021, 33 (1): 16- 22. doi: 10.1097/CCO.0000000000000695
3	Brönimann S , Garstka N , Remzi M . Treatment of adrenocortical carcinoma: Oncological and endocrine outcomes[J]. Curr Opin Urol, 2023, 33 (1): 50- 58. doi: 10.1097/MOU.0000000000001045
4	Xu WH , Wu J , Wang J , et al. Screening and identification of potential prognostic biomarkers in adrenocortical carcinoma[J]. Front Genet, 2019, 10, 821. doi: 10.3389/fgene.2019.00821
5	邓建华, 李汉忠, 纪志刚, 等. 肾上腺皮质癌的综合治疗[J]. 北京大学学报(医学版), 2019, 51 (2): 298- 301.
6	Quinones-Baldrich W , Alktaifi A , Eilber F , et al. Inferior vena cava resection and reconstruction for retroperitoneal tumor excision[J]. J Vasc Surg, 2012, 55 (5): 1386- 1393. doi: 10.1016/j.jvs.2011.11.054
7	Schwarzbach MH , Hormann Y , Hinz U , et al. Clinical results of surgery for retroperitoneal sarcoma with major blood vessel involvement[J]. J Vasc Surg, 2006, 44 (1): 46- 55. doi: 10.1016/j.jvs.2006.03.001
8	Nooromid MJ , Ju MH , Havelka GE , et al. Fifteen-year expe-rience with renal cell carcinoma with associated venous tumor thrombus[J]. Surgery, 2016, 160 (4): 915- 923. doi: 10.1016/j.surg.2016.06.029
9	Shao P , Li J , Qin C , et al. Laparoscopic radical nephrectomy and inferior vena cava thrombectomy in the treatment of renal cell carcinoma[J]. Eur Urol, 2015, 68 (1): 115- 122. doi: 10.1016/j.eururo.2014.12.011
10	Agochukwu N , Shuch B . Clinical management of renal cell carcinoma with venous tumor thrombus[J]. World J Urol, 2014, 32 (3): 581- 589. doi: 10.1007/s00345-014-1276-7
11	Fairweather M , Raut CP . Nephrectomy for retroperitoneal sarcoma: Stay calm and (cautiously) carry on[J]. Ann Surg Oncol, 2021, 28 (3): 1275- 1277. doi: 10.1245/s10434-020-09293-w
12	Liu Z , Ge L , Liu L , et al. Clinical experience and management strategy of retroperitoneal tumor with venous tumor thrombus involvement[J]. Front Oncol, 2022, 12, 873729. doi: 10.3389/fonc.2022.873729
13	Jannello LMI, Incesu RB, Morra S, et al. The European Network for the Study of Adrenal Tumors staging system (2015): A United States validation[J/OL]. J Clin Endocrinol Metab, 2024: dgae047[2024-02-18]. doi: 10.1210/clinem/dgae047.
14	Liu Z , Zhao X , Ge L , et al. Completely laparoscopic versus open radical nephrectomy and infrahepatic tumor thrombectomy: Comparison of surgical complexity and prognosis[J]. Asian J Surg, 2021, 44 (4): 641- 648. doi: 10.1016/j.asjsur.2020.12.003
15	Zhang G , Li X , Sun G , et al. Clinical analysis of Kimura's di-sease in 24 cases from China[J]. BMC Surg, 2020, 20 (1): 1. doi: 10.1186/s12893-019-0673-7
16	Liu Z , Li Y , Zhang Y , et al. PUTH grading system for urinary tumor with supradiaphragmatic tumor thrombus: Different surgical techniques for different tumor characteristics[J]. Front Oncol, 2022, 11, 735145. doi: 10.3389/fonc.2021.735145
17	Blute ML , Leibovich BC , Lohse CM , et al. The Mayo clinic experience with surgical management, complications and outcome for patients with renal cell carcinoma and venous tumour thrombus[J]. BJU Int, 2004, 94 (1): 33- 41. doi: 10.1111/j.1464-410X.2004.04897.x
18	Laan DV , Thiels CA , Glasgow A , et al. Adrenocortical carcinoma with inferior vena cava tumor thrombus[J]. Surgery, 2017, 161 (1): 240- 248. doi: 10.1016/j.surg.2016.07.040
19	Piardi T , Lhuaire M , Memeo R , et al. Laparoscopic Pringle maneuver: How we do it?[J]. Hepatobiliary Surg Nutr, 2016, 5 (4): 345- 349. doi: 10.21037/hbsn.2015.11.01
20	Fiore M , Colombo C , Locati P , et al. Surgical technique, morbi-dity, and outcome of primary retroperitoneal sarcoma involving inferior vena cava[J]. Ann Surg Oncol, 2012, 19 (2): 511- 518. doi: 10.1245/s10434-011-1954-2
21	刘磊, 王国良, 马潞林, 等. 肾上腺区巨大肿瘤合并瘤栓的诊断与治疗[J]. 北京大学学报(医学版), 2019, 51 (4): 684- 688.
22	杨华安, 郭胜杰. 肾上腺皮质癌合并静脉癌栓的手术治疗及预后[J]. 实用医学杂志, 2020, 36 (10): 1344- 1348. doi: 10.3969/j.issn.1006-5725.2020.10.015
23	Zhao X , Liu Z , Zhang H , et al. PKUTHLP score: A comprehensive system to predict surgical approach in radical nephrectomy and thrombectomy[J]. Oncol Lett, 2020, 20 (1): 201- 208. doi: 10.3892/ol.2020.11571
24	Vuong NS , Ferriere JM , Michiels C , et al. Robot-assisted versus open surgery for radical nephrectomy with level 1-2 vena cava tumor thrombectomy: A French monocenter experience (UroCCR study #73)[J]. Minerva Urol Nephrol, 2021, 73 (4): 498- 508.
25	Treiger BF , Humphrey LS , Peterson CV , et al. Transesophageal echocardiography in renal cell carcinoma: An accurate diagnostic technique for intracaval neoplastic extension[J]. J Urol, 1991, 145 (6): 1138- 1140. doi: 10.1016/S0022-5347(17)38556-7

相关文章 15

[1]	欧俊永,倪坤明,马潞林,王国良,颜野,杨斌,李庚午,宋昊东,陆敏,叶剑飞,张树栋. 肌层浸润性膀胱癌合并中高危前列腺癌患者的预后因素[J]. 北京大学学报（医学版）, 2024, 56(4): 582-588.
[2]	虞乐,邓绍晖,张帆,颜野,叶剑飞,张树栋. 具有低度恶性潜能的多房囊性肾肿瘤的临床病理特征及预后[J]. 北京大学学报（医学版）, 2024, 56(4): 661-666.
[3]	周泽臻,邓绍晖,颜野,张帆,郝一昌,葛力源,张洪宪,王国良,张树栋. 非转移性T_3a肾细胞癌患者3年肿瘤特异性生存期预测[J]. 北京大学学报（医学版）, 2024, 56(4): 673-679.
[4]	方杨毅,李强,黄志高,陆敏,洪锴,张树栋. 睾丸鞘膜高分化乳头状间皮肿瘤1例[J]. 北京大学学报（医学版）, 2024, 56(4): 741-744.
[5]	曾媛媛,谢云,陈道南,王瑞兰. 脓毒症患者发生正常甲状腺性病态综合征的相关因素[J]. 北京大学学报（医学版）, 2024, 56(3): 526-532.
[6]	苏俊琪,王晓颖,孙志强. 舌鳞状细胞癌根治性切除术后患者预后预测列线图的构建与验证[J]. 北京大学学报（医学版）, 2024, 56(1): 120-130.
[7]	李建斌,吕梦娜,池强,彭一琳,刘鹏程,吴锐. 干燥综合征患者发生重症新型冠状病毒肺炎的早期预测[J]. 北京大学学报（医学版）, 2023, 55(6): 1007-1012.
[8]	刘欢锐,彭祥,李森林,苟欣. 基于HER-2相关基因构建风险模型用于膀胱癌生存预后评估[J]. 北京大学学报（医学版）, 2023, 55(5): 793-801.
[9]	薛子璇,唐世英,邱敏,刘承,田晓军,陆敏,董靖晗,马潞林,张树栋. 青年肾肿瘤伴瘤栓的临床病理特征及预后分析[J]. 北京大学学报（医学版）, 2023, 55(5): 802-811.
[10]	兰东,刘茁,李宇轩,王国良,田晓军,马潞林,张树栋,张洪宪. 根治性肾切除和静脉癌栓取出术大出血的危险因素[J]. 北京大学学报（医学版）, 2023, 55(5): 825-832.
[11]	卢汉,张建运,杨榕,徐乐,李庆祥,郭玉兴,郭传瑸. 下颌牙龈鳞状细胞癌患者预后的影响因素[J]. 北京大学学报（医学版）, 2023, 55(4): 702-707.
[12]	时云飞,王豪杰,刘卫平,米岚,龙孟平,刘雁飞,赖玉梅,周立新,刁新婷,李向红. 血管免疫母细胞性T细胞淋巴瘤临床与分子病理学特征分析[J]. 北京大学学报（医学版）, 2023, 55(3): 521-529.
[13]	朱晓娟,张虹,张爽,李东,李鑫,徐玲,李挺. 人表皮生长因子受体2低表达乳腺癌的临床病理学特征及预后[J]. 北京大学学报（医学版）, 2023, 55(2): 243-253.
[14]	赖玉梅,李忠武,李欢,吴艳,时云飞,周立新,楼雨彤,崔传亮. 68例肛管直肠黏膜黑色素瘤临床病理特征及预后[J]. 北京大学学报（医学版）, 2023, 55(2): 262-269.
[15]	沈棋,刘亿骁,何群. 肾黏液样小管状和梭形细胞癌的临床病理特点及预后[J]. 北京大学学报（医学版）, 2023, 55(2): 276-282.

Metrics

Viewed

Full text

Abstract

Cited

Shared

Discussed

Feature	With tumor thrombus (n=11)	Without tumor thrombus (n=16)	P value
Age/years	49 (36, 58)	48 (37, 62)	0.8
Female	8 (72.7)	7 (56.3)	0.4
BMI/(kg/m²)	26.0 (24.1, 30.4)	25.1 (23.3, 27.6)	0.3
Clinical symptoms			0.3
No	4 (36.4)	11 (68.8)
Local symptoms	5 (45.5)	3 (18.8)
Systemic symptoms	2 (18.2)	2 (12.5)
Hypercortisolism	2 (18.2)	2 (12.5)	1.0
Hypertension	6 (54.5)	6 (37.5)	0.5
Side			0.5
Left	3 (27.3)	7 (43.8)
Right	8 (72.7)	8 (50.5)
Bilateral	0	1 (6.3)
Tumor size/cm	9.4 (6.5, 12.5)	10.5 (6.1, 13.0)	1.0
ENSAT stage			0.1
Ⅰ	0	2 (12.5)
Ⅱ	0	4 (25.0)
Ⅲ	10 (90.9)	9 (56.3)
Ⅳ	1 (9.1)	1 (6.3)
pN1	1 (9.1)	2 (12.5)	1.0
M1	1 (9.1)	1 (6.3)	1.0
Thrombus length/cm	3.0 (1.6, 4.0)
Mayo grade
0	2 (18.2)
Ⅰ	2 (18.2)
Ⅱ	6 (54.5)
Ⅲ	1 (9.1)
PUTH-RT grading system
1a	2 (18.2)
2	6 (54.5)
3	3 (27.3)
Operative time/min	332.0 (261.0, 440.0)	223.5 (137.8, 308.5)	0.08
Estimated blood loss/mL	900 (700, 2 200)	450 (20, 1 200)	0.09
Patients receiving transfusion	7 (63.6)	8 (50.0)	0.7
Postoperative hospital stay/d	9 (5, 10)	8 (6, 12)	0.9
Postoperative complication	4 (36.4)	4 (25.0)	0.7

Patient	PUTH-RT grade	Mayo grade	Age/years	Gender	BMI/(kg/m²)	Hypertension	Symptoms	Side	Diameter/cm	ENSAT stage	cT stage	cN stage	cM stage	Thrombus length/cm
1	3	Ⅲ	31	F	30.4	No	Local	R	15.0	Ⅲ	T3	N0	M0	5.0
2	2	Ⅰ	58	M	24.1	Yes	No	R	9.4	Ⅲ	T3	N0	M0	3.0
3	2	Ⅱ	56	F	36.2	Yes	No	R	6.5	Ⅲ	T3	N0	M0	4.0
4	2	Ⅱ	49	F	21.5	No	Local	L	12.2	Ⅲ	T4	N0	M0	4.0
5	2	Ⅱ	54	F	26.0	No	No	R	7.1	Ⅲ	T3	N0	M0	3.3
6	3	Ⅱ	69	F	23.1	Yes	Systemic	R	12.5	Ⅳ	T3	N1	M1	3.0
7	1a	0	71	F	26.9	Yes	No	R	4.5	Ⅲ	T3	N0	M0	0.5
8	1a	0	39	M	24.9	No	Local	L	12.0	Ⅲ	T3	N0	M0	0.8
9	2	Ⅱ	23	F	27.7	No	Local	L	16.3	Ⅲ	T4	N0	M0	2.8
10	3	Ⅱ	36	M	24.5	Yes	Local	R	8.3	Ⅲ	T3	N0	M0	2.5
11	2	Ⅰ	49	F	35.9	Yes	Systemic	R	5.5	Ⅲ	T3	N0	M0	1.6

Patient	Operation approach	Operative time/min	Blood loss/mL	RCS transfusion/mL	LN resection	Hospital stay/d	Complication	Follow-up/months	Status	Recurrence
1	Open	504	3 500	3 200	No	9	Anemia	14.0	Dead	Liver, lung, retroperitoneal
2	Laparoscopic	193	200	0	No	5		12.0	Dead	Liver, lung
3	Laparoscopic	335	800	400	No	8		9.0	Dead	Liver, lung, retroperitoneal
4	Open	440	2 000	1 600	Yes	9		20.0	Dead	Diaphragmatic, lymph node
5	Laparoscopic	261	900	0	No	5		11.0	Dead	Liver, lung, retroperitoneal
6	Open	355	3 500	2 800	Yes	10		9.0	Dead	Liver
7	Laparoscopic	71	10	0	No	3		24.0	Dead	Liver, lung
8	Robot	332	700	0	No	12	Ascites	32.0	Alive
9	Open	477	2 200	1 600	Yes	13	Anemia	19.0	Dead	Lung
10	Open	322	1 500	800	No	10	Infection	15.0	Alive	Lung
11	Open	282	800	400	No	10		14.0	Alive	Lung