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王淼, 刘明, 张伟, 朱生才, 张耀光, 张大磊, 王萱, 王建业. 中高危局限性前列腺癌患者扩大盆腔淋巴结清扫的初步临床研究成果分析[J]. 微创泌尿外科杂志, 2019,8(5): 334-339.
WANG Miao, LIU Ming, ZHANG Wei, ZHU Shengcai, ZHANG Yaoguang, ZHANG Dalei, WANG Xuan, WANG Jianye. A clinical study on extended pelvic lymph node dissection of Chinese patients with intermediate-high risk localized prostate cancer——An analysis of preliminary data. JOURNAL OF MINIMALLY INVASIVE UROLOGY,2019,8(5): 334-339.  
Doi:10.19558/j.cnki.10-1020/r.2019.05.010
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中高危局限性前列腺癌患者扩大盆腔淋巴结清扫的初步临床研究成果分析
王淼1,2, 刘明1, 张伟3, 朱生才1, 张耀光1, 张大磊1, 王萱1, 王建业1
1北京医院国家老年医学中心泌尿外科 100730北京
2北京协和医学院研究生院
3北京医院国家老年医学中心病理科
通信作者：刘明,liuming19731029@163.com
收稿日期: 2019-01-02
基金项目:首都临床特色应用研究（Z171100001017201）
摘要

目的：对中高危局限性前列腺癌患者扩大盆腔淋巴结清扫的淋巴结阳性率进行研究,并探讨影响阳性率的潜在因素。方法：对2014年3月–2018年6月于北京医院行根治性前列腺切除术及扩大盆腔淋巴结清扫术的32例患者资料进行回顾性研究。入组患者均为中高危局限性前列腺癌患者,年龄56~78岁,中位年龄68.5岁。术前PSA 5.17~180.15 μg/L,中位PSA 20.52 μg/L,术前穿刺Gleason评分6~10分,中位评分7分。中危组患者4例,高危组患者28例。对患者先行腹腔镜扩大盆腔淋巴结清扫术,再行前列腺根治性切除术,将所取的淋巴结分区送检。结果：术中共切除淋巴结455枚,每例患者清扫淋巴结6~27枚,中位数12.5枚,32例患者中有4例发现阳性淋巴结,阳性率为12.5%。4例淋巴结阳性患者均来自高危组,术前PSA>20 μg/L且Gleason评分≥7分,术后病理分期pT3bN1M0,其中2例患者阳性淋巴结位于闭孔区域,1例患者分布于闭孔及髂内动脉旁,1例患者分布于闭孔、髂外及髂内动脉旁区域。6例患者出现术后并发症,总并发症发生率为18.75%,其中3例考虑与扩大盆腔淋巴结清扫特异相关,发生率为9.4%。结论：对于中高危局限性前列腺癌患者,穿刺Gleason 评分≥7分、术前PSA>20 μg/L提示更高的淋巴结侵犯可能。中高危局限性前列腺癌患者扩大盆腔淋巴结清扫适应证、其治疗意义以及国内外患者人群的淋巴结转移特点是否存在差异还需要进一步研究证明。

关键词: 前列腺癌; 淋巴结转; 淋巴结清扫; 前列腺切除术
中图分类号:R737.25 文献标志码:A
A clinical study on extended pelvic lymph node dissection of Chinese patients with intermediate-high risk localized prostate cancer——An analysis of preliminary data
WANG Miao1,2, LIU Ming1, ZHANG Wei3, ZHU Shengcai1, ZHANG Yaoguang1, ZHANG Dalei1, WANG Xuan1, WANG Jianye1
1Department of Urology, Beijing Hospital, National Center of Gerontology, Beijing 100730, China
2Graduate School of Peking Union Medical College
3Department of Pathology, Beijing Hospital, National Center of Gerontology
Corresponding author： LIU Ming, liuming19731029@163.com
Abstract

Objective： To determine the incidence of pelvic lymph node involvement and the complication rate of extended pelvic lymphadenectomy in a group of Chinese patients and to investigate the underlying prediction factors.Methods: A total of 32 consecutive patients with intermediate-high risk localized prostate cancer who underwent laparoscopic radical prostatectomy (RP) and extended pelvic lymph node dissection (ePLND) during March, 2014 and June, 2018 in Beijing Hospital were retrospectively studied. The age of patients ranged from 56-78 years with a median age of 68.5 years. Pre-operation PSA level ranged from 5.17 to 180.15 μg/L with a median level of 20.52 μg/L. The Gleason score ranged from 6 to 10 with the median score of 7. Of those 32 patients, 4 were from intermediate risk group, and 17 were from high risk group. EPLND was performed first before radical prostatectomy. The template of the lymph node dissection included the genitofemoral nerve anterolaterally, the internal iliac artery posteromedially, the bifurcation of the common iliac artery cranially, and the origin of the epigastric vessels caudally. Lymph nodes were sent by separate packages to maximize lymph node inspection.Results: A total of 455 lymph nodes were removed with a median number of lymph nodes removed from each patient of 12.5 (ranging from 6 to 27). Of all 32 patients, 4 were found with lymph node invasion (LNI), giving a positive rate of 12.5%. The four patients with LNI were all from high risk group, with a pre-operation PSA level over 20 μg/L, biopsy Gleason score not less than 7, and a pathologic stage of T3bN1M0. Metastases were identified in all three regions, with two patients within obturator region, one in internal iliac and obturator region and one in internal iliac, external iliac and obturator region. Six patients had complications after surgery, giving a complication rate of 18.75%. Three of these complications have been attributed to nodal dissection, giving a rate of 9.4%.Conclusion: Extended pelvic lymph node dissection at the time of RP is a reliable diagnostic procedure to achieve more pathohistological staging information. It seems that patients from high risk group with a pre-operation PSA level over 20 μg/L, biopsy Gleason score not less than 7 tend to be more likely to have positive lymph nodes detected with ePLND. Further research is required to investigate more accurate positive rate and prediction factors for Chinese patients, as well as the therapeutic role of ePLND.

Keyword: prostate neoplasm; lymphatic metastases; lymph node excision; prostatectomy

盆腔淋巴结清扫是前列腺癌根治性切除术中的重要步骤, 同时也是目前检测和清除淋巴结微小转移病灶最可靠的方法, 一直被认为是前列腺癌病理分期中判断淋巴结转移的金标准[1, 2]。

近期研究认为, 前列腺的淋巴引流复杂, 除闭孔淋巴结外, 髂内动脉旁淋巴结、骶前淋巴结甚至髂总动脉旁淋巴结都可能成为淋巴转移的第一站, 因此单纯行闭孔淋巴结活检, 可能会造成假阴性并遗留淋巴微转移病灶[3]。越来越多的研究表明淋巴结阳性发生率与术中清扫淋巴结数目存在正相关, 术中扩大盆腔淋巴结清扫范围会提高手术病理分期的精确度[4, 5, 6]。同时, 有回顾性研究提出, 扩大盆腔淋巴结清扫范围可清除微转移病灶, 存在潜在的治疗效果, 但仍有待进一步研究证实[6, 7, 8, 9]。

目前国内指南同欧洲指南一致建议：对术前预测淋巴结受累风险大于5%的患者行根治性手术的同时进行扩大盆腔淋巴结清扫术[1]。但是, 各中心在实际诊治过程中并没有形成统一的标准。与此同时, 对于国内患者淋巴结转移特点、手术阳性率以及影响阳性率的预测因素鲜有报道。我们通过对北京医院国家老年医学中心接受扩大盆腔淋巴结清扫术的局限性中高危前列腺癌患者进行回顾性研究, 旨在总结国内局限性前列腺癌患者淋巴结转移的阳性率、影响因素、及手术中相关并发症出现情况。

1 资料与方法
1.1 临床资料

选取北京医院2014年3月– 2018年6月期间接受腹腔镜经腹腔途径根治性前列腺切除及扩大盆腔淋巴结清扫术的32例中高危局限性前列腺癌患者资料进行回顾性研究。其中, 中危组患者4例, 高危组患者28例。前列腺癌危险分层采用2017年EAU指南危险分层标准[1], 即低危：PSA< 10 μ g/L和Gleason评分< 7且cT1~2a; 中危：PSA 10~20 μ g/L或Gleason评分=7或cT2b; 高危：PSA> 20 μ g/L或Gleason评分> 7或cT2c。入组患者年龄56~78岁, 中位年龄68.5岁。术前PSA 5.17~180.15 μ g/L, 中位PSA 20.52 μ g/L, 术前穿刺Gleason评分6~10分, 中位评分7分。详见表1。本研究均报请并通过医院伦理委员会审核。

表1 患者基本情况
1.2 手术方法

32例患者均接受腹腔镜经腹腔途径根治性前列腺切除及扩大盆腔淋巴结清扫术。术中先行扩大盆腔淋巴结清扫术, 再行根治性前列腺切除术。盆腔淋巴结清扫由髂总动脉分叉处开始, 分别切除两侧髂外动脉旁淋巴结、闭孔淋巴结及髂内动脉旁淋巴结。清扫范围如下：外界为生殖股神经, 内界为髂内动脉, 上界为髂总动脉分叉处, 下界为腹壁动静脉起始处（图1）。分区送检所取的淋巴结（部分患者髂内动脉旁和闭孔两组淋巴结分离困难, 术中合为一组送检, 并单独送检髂外动脉旁淋巴结）。所送标本行5 mm连续切片检查, 对疑似受侵犯的淋巴结组织全部进行镜检及免疫组化检查。

图 1 盆腔淋巴结的分布区域及手术范围
1：髂外动脉旁区域; 2：闭孔淋巴结区域; 3髂内动脉旁区域。

1.3 统计学方法

限于患者例数, 本研究仅采用描述性数据分析。

2 结果

32例患者全部接受扩大盆腔淋巴结清扫, 术中共切除淋巴结455枚, 每例患者切除淋巴结6~27枚, 中位数目12.5枚, 其中4例患者发现阳性淋巴结, 淋巴结阳性检出率为12.5%。阳性淋巴结在闭孔、髂外及髂内动脉旁区域均有分布。4例阳性患者均来自高危组, 术前PSA> 20 μ g/L, 术前穿刺Gleason评分≥ 7分, 术后病理分期pT3bN1M0, 患者穿刺阳性针数百分比分别为66.7%、35.3%、58.3%, 40.0%。详见表2。

表2 淋巴结阳性患者基本信息

32例患者术中均未出现严重出血、神经损伤等并发症, 术后6例患者出现并发症, 术后总并发症发生率18.75%。对患者伤口引流管、尿管留置时间、引流量以及引流液性质进行评估, 3例患者出现尿瘘, 2例患者出现淋巴瘘, 1例患者出现淋巴瘘及下肢会阴部水肿, 未出现深静脉血栓、肺栓塞等其他文献报道的并发症。考虑淋巴瘘及淋巴水肿的发生可能与扩大盆腔淋巴结清扫手术特异性相关, 其发生率为9.4%。据改良版Clavien手术并发症分级方法[10]对术后出现并发症患者进行分级, 6例患者出现的并发症均属于I级。

3 讨论

对局限性前列腺癌患者是否进行盆腔淋巴结清扫一直广受争议。一方面是由于目前尚缺乏前瞻性随机对照研究评估, 无法证明扩大盆腔淋巴结清扫给患者带来的获益及负面风险; 另一方面盆腔淋巴结清扫的范围亦未能达到共识。

目前, 关于前列腺癌盆腔淋巴结清扫范围主要可以分为三大类：局限性盆腔淋巴结清扫（limited pelvic lymph node dissection, lPLND）, 清扫范围包含闭孔淋巴结, 含或不含髂外动脉旁淋巴结; 标准盆腔淋巴结清扫（standard pelvic lymph node dissection, sPLND）, 清扫范围包括闭孔淋巴结及髂外动脉旁淋巴结; 扩大盆腔淋巴结清扫（extended pelvic lymph node dissection, ePLND）, 其清扫范围并没有达成共识, 但目前主流观点认为应清扫范围应至少包含闭孔淋巴结、髂外动脉旁淋巴结、髂内动脉旁淋巴结在内的区域淋巴结[1, 2, 11], 这样可以清除前列腺引流区域63%的淋巴结[5]。Mattei等[3]则推荐可以扩大清扫范围至髂总动脉与输尿管交叉处, 这样可以清除前列腺引流区域75%的淋巴结。越来越多的研究证实闭孔淋巴结并非前列腺癌淋巴转移确切的“ 第一站” , Bader等[12]报道的淋巴结转移患者中, 有高达19%的转移灶位于髂内动脉旁淋巴结。因此, 传统的闭孔淋巴结活检, 或者仅行闭孔淋巴结加髂外动脉旁淋巴结的盆腔淋巴结清扫, 很可能造成假阴性结果, 从而影响手术病理分期的准确性, 并有遗留微转移病灶的风险。已有对比局限性盆腔淋巴结清扫和扩大盆腔淋巴结清扫的研究结果证明, 后者术中切除淋巴结的平均数目大约是前者的2倍, 而淋巴结阳性率可以达到前者的2~3倍, 可能提示淋巴结阳性检出率与切除淋巴结数目呈正相关[4, 5]。Weingartner等[13]发现术中平均切除20枚淋巴结可以较为准确地反映淋巴结转移情况。对于中高危前列腺癌患者进行扩大盆腔淋巴结清扫, Stone等[4]报道了23.2%的阳性率, 而Heidenreich等[5]报道了27%的阳性率。有研究表明, 对于低危、中危和高危局限性前列腺癌患者进行扩大盆腔淋巴结清扫, 分别可以获得5%~6%、20%~25%及30%~40%的阳性率, 对比局限性盆腔淋巴结清扫的结果差异有统计学意义[1]。因此, 多项研究推荐对于淋巴结侵犯可能性较高的中高危前列腺癌患者, 应选择进行扩大盆腔淋巴结清扫[2, 14, 15, 16, 17, 18]。

本研究中每位患者所切取淋巴结数目（6~27）枚, 中位数目12.5枚, 淋巴结阳性检出率12.5%, 结果明显低于国外报道平均水平, 这可能与最终获得淋巴结数目偏少相关。根据文献报道, 前列腺癌扩大盆腔淋巴结清扫术中切除的淋巴结数目平均为21~28枚, 局限性清扫中切除的淋巴结数目平均为10~11枚[4, 5, 19, 20, 21]。此外, 由于部分患者在术中未达到淋巴结完全分区送检的要求, 而病理科医生采用传统手检淋巴结也具有一定的局限性, 因此在国外的相关研究中, 对于术后所取组织先用丙酮溶解脂肪, 再将淋巴结全部取材, 以便找到更多的淋巴结[12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22]。但是国内中高危局限性前列腺癌患者淋巴结转移阳性率是否与国外患者人群存在客观差异, 目前尚不清楚。因此国内患者淋巴转移阳性率及相关影响因素也是本研究的方向。本研究中发现4例淋巴结阳性患者, 阳性淋巴结位置除了出现在常见的闭孔淋巴结区域, 还有1例患者出现在髂内动脉旁区域, 1例同时分布于闭孔、髂内及髂外动脉旁区域, 这也提示传统单纯行闭孔淋巴结活检的确可能造成假阴性并遗留淋巴结转移病灶。

关于前列腺癌术前淋巴结转移的预测, 目前有不同的预测模型和量表。这些预测量表一般都将术前PSA水平、术前临床分期、术前穿刺Gleason评分等变量作为预测淋巴结侵犯风险的指标。但是现有预测模型大都以行局限性盆腔淋巴结清扫的患者数据作为研究资料, 因此预测的侵犯风险可能要低于实际的阳性风险。Briganti等[23]以扩大盆腔淋巴结清扫患者数据为研究资料制作了预测模型, 被作为目前欧洲和国内指南预测淋巴结侵犯风险的参考模型。有预测模型增加了穿刺阳性针数比例这项变量, 因其在一定程度上可能代表着肿瘤负荷, 也被认为与淋巴结侵犯风险关系最为密切, 其相关性也在一系列研究中被证实[11, 22]。本研究对术前PSA水平、术前临床分期、穿刺Gleason评分以及穿刺阳性针数所占比例等因素进行分析, 限于入组患者例数, 无法得出具有统计学差异的结果, 但是总结4例淋巴结阳性患者的共同特点, 考虑术前PSA> 20 μ g/L、穿刺Gleason评分≥ 7分的高危前列腺癌患者, 行扩大盆腔淋巴结清扫可能会有更高的阳性率。本研究中4例阳性患者阳性针数比例分别为66.7%、35.3%、58.3%, 40.0%, 相比于阴性患者未发现明显比例更高的趋势, 这可能也是受到患者数目过少的影响。

前列腺癌盆腔淋巴结清扫并发症发生率为5%~35%[24, 25, 26]。Rousseau等[26]研究证实扩大盆腔淋巴结清扫会导致更高的并发症发生率, 但是部分研究结果却提示, 局限性以及扩大盆腔淋巴结清扫在术中及术后并发症发生率以及严重程度方面并无显著差异[5, 6, 8]。目前主流观点认为扩大盆腔淋巴结清扫会导致更高的并发症发生率, 该观点也得到了系统性评价资料的证实[27]。但Morizane等[28]最近在日本开展的一项多中心回顾性研究发现并发症发生率与手术操作时间最为相关, 与淋巴结清扫范围并无显著相关性。而在发生的并发症类型中, 淋巴囊肿最为常见, 其他并发症如深静脉血栓、肺栓塞、下肢淋巴水肿、闭孔神经以及输尿管的损伤发生率相对较低[2]。本研究术中无并发症发生, 术后共有6例患者出现并发症, Clavien分级均为I级, 其中与扩大盆腔淋巴结清扫相关并发症（微淋巴瘘及水肿）发生率为9.4%。扩大盆腔淋巴结清扫手术相关并发症可以通过术中精细操作, 提高手术技术在一定程度上得到避免, 在有经验的中心并发症发生率并不高。

本研究局限性在于入组患者例数过少, 使得数据结果可能存在较大偏倚, 无法完全反映真实水平, 同时不能得出具有统计学差异的结果。

综上所述, 中高危局限性前列腺癌患者行扩大盆腔淋巴结清扫可以获得更加精确的病理分期, 并且可能获得潜在的治疗受益。术前PSA> 20 μ g/L, 穿刺Gleason评分≥ 7分的高危前列腺癌患者行扩大盆腔淋巴结清扫可能获得更高的淋巴结阳性率。本研究发现淋巴结阳性率为10%, 低于国外报道水平。明确国内中高危局限性前列腺癌患者扩大盆腔淋巴结清扫适应证、其治疗意义以及国内患者淋巴结转移与国外患者是否存在差异还需要进一步研究证明。

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