Abstract
目的
评估基于MRI前列腺腺体相关参数构建的列线图预测腹腔镜前列腺癌术后尿失禁的临床价值。
方法
纳入经前列腺穿刺活检诊断为前列腺腺癌并于北京大学第三医院行腹腔镜根治性前列腺切除术(laparo-scopic radical prostatectomy，LRP)的202例患者，所有患者的术前MRI检查于前列腺穿刺活检术前1周内完成，腺体相关参数包含前列腺上下径、左右径、前后径、前列腺体积、前列腺尖部突入深度(intravesical prostatic protrusion length，IPPL)、前列腺尖部形态分型等。自术后第1个月起，每个月对患者的控尿功能恢复情况进行随访，以全天不需要使用尿垫作为控尿功能恢复标准。应用Logistic多因素回归分析影响术后早期控尿功能恢复的危险因素，绘制各模型预测术后控尿功能恢复的受试者操作特征(receiver operator characteristic，ROC)曲线，以DeLong检验比较曲线下面积的差异，以决策曲线分析评价模型的临床净获益。
结果
202例患者的平均年龄为69.0(64.0, 75.5)岁，穿刺前平均前列腺特异性抗原(prostate specific antigen，PSA)为12.12 (7.36, 20.06) μg/L，穿刺Gleason评分 < 7分和≥7分者分别为73例(36.2%)和129例(63.9%)，临床分期为T1/T2期者100例(49.5%)，T3期者102例(50.5%)。经术前MRI测量，前列腺体积为35.4 (26.2, 51.1) mL，前列腺上下径与左右径的比值为0.91 (0.77, 1.07)，膜性尿道长度为15 (11, 16) mm，IPPL为2 (0, 6) mm，前列腺尖部形态分型A~D型分别为67例(33.2%)、80例(39.6%)、24例(11.9%)和31例(15.3%)，训练集和验证集分别为141例和61例。所有患者手术均顺利完成，随访3个月患者的控尿率为59.4%(120/202例)。训练集多因素分析结果显示，膜性尿道长度(P < 0.001)、IPPL(P=0.017)和临床分期(P=0.022)是术后早期(3个月)尿失禁发生的独立危险因素。根据多因素分析结果制作列线图和临床决策曲线，计算训练集ROC曲线下面积为0.885 (0.826, 0.944)，计算验证集ROC曲线下面积为0.854 (0.757, 0.950)。在验证集里对模型进行Hosmer-Lemeshow拟合优度检验，卡方值为5.426 (P=0.711)。
结论
术前膜性尿道长度、IPPL、临床分期是LRP术后早期尿失禁发生的独立危险因素，基于MRI前列腺腺体相关参数构建的列线图可有效预测LRP术后早期控尿功能恢复，但此结果还需更大规模的临床研究证实。
Keywords: 前列腺肿瘤, 控尿功能, 腹腔镜手术, 前列腺切除术, 列线图
Abstract
Objective
Constructing a predictive model for urinary incontinence after laparoscopic radical prostatectomy (LRP) based on prostatic gland related MRI parameters.
Methods
In this study, 202 cases were included. All the patients were diagnosed with prostate cancer by prostate biopsy and underwent LRP surgery in Peking University Third Hospital. The preoperative MRI examination of all the patients was completed within 1 week before the prostate biopsy. Prostatic gland related parameters included prostate length, width, height, prostatic volume, intravesical prostatic protrusion length (IPPL), prostate apex shape, etc. From the first month after the operation, the recovery of urinary continence was followed up every month, and the recovery of urinary continence was based on the need not to use the urine pad all day long. Logistic multivariate regression analysis was used to analyze the influence of early postoperative recovery of urinary continence. Risk factors were used to draw the receiver operator characteristic (ROC) curves of each model to predict the recovery of postoperative urinary continence, and the difference of the area under the curve (AUC) was compared by DeLong test, and the clinical net benefit of the model was evaluated by decision curve analysis (DCA).
Results
The average age of 202 patients was 69.0 (64.0, 75.5) years, the average prostate specific antigen (PSA) before puncture was 12.12 (7.36, 20.06) μg/L, and the Gleason score < 7 points and ≥ 7 points were 73 cases (36.2%) and 129 cases (63.9%) respectively, with 100 cases (49.5%) at T1/T2 clinical stage, and 102 cases (50.5%) at T3 stage. The prostatic volume measured by preoperative MRI was 35.4 (26.2, 51.1) mL, the ratio of the height to the width was 0.91 (0.77, 1.07), the membranous urethral length (MUL) was 15 (11, 16) mm, and the IPPL was 2 (0, 6) mm. The prostatic apex A-D subtypes were 67 cases (33.2%), 80 cases (39.6%), 24 cases (11.9%) and 31 cases (15.3%), respectively. The training set and validation set were 141 cases and 61 cases, respectively. The operations of all the patients were successfully completed, and the urinary continence rate was 59.4% (120/202) in the 3 months follow-up. The results of multivariate analysis of the training set showed that the MUL (P < 0.001), IPPL (P=0.017) and clinical stage (P=0.022) were independent risk factors for urinary incontinence in the early postoperative period (3 months). The nomogram and clinical decision curve were made according to the results of multivariate analysis. The AUC value of the training set was 0.885 (0.826, 0.944), and the AUC value of the validation set was 0.854 (0.757, 0.950). In the verification set, the Hosmer-Lemeshow goodness-of-fit test was performed on the model, and the Chi-square value was 5.426 (P=0.711).
Conclusion
Preoperative MUL, IPPL, and clinical stage are indepen-dent risk factors for incontinence after LRP. The nomogram developed based on the relevant parameters of MRI glands can effectively predict the recovery of early urinary continence after LRP. The results of this study require further large-scale clinical research to confirm.
Keywords: Prostate neoplasm, Urinary continence, Laparoscopic surgery, Prostatectomy, Nomogram
前列腺根治性切除术是治疗局限性和局部晚期前列腺癌的标准方法[1]，尿失禁是术后最常见的并发症之一。接受前列腺根治性切除术后，绝大部分患者的尿失禁在1年内恢复，但术后早期尿失禁仍然严重影响患者的生活质量[2-3]。前列腺根治性切除术后尿失禁的影响因素包含患者自身情况、术者经验、肿瘤情况和手术技术等[4]，采用术前解剖学因素预测术后控尿功能恢复是近年来前列腺癌手术治疗领域的研究热点[5-6]，目前研究的解剖学因素主要包含括约肌相关参数、腺体相关参数、盆底支持结构和骨盆相关参数等，膜性尿道长度(membranous urethral length, MUL)作为重要的括约肌相关参数已被一项荟萃分析证实是前列腺根治性切除术后控尿功能恢复的独立危险因素[7]。盆腔MRI检查的前列腺腺体相关参数[如前列腺体积、前列腺尖部突入深度(intravesical prostatic protrusion length，IPPL)、前列腺尖部形态分型等]与手术难度、并发症发生风险、神经血管束保留及术后功能学预后存在相关性。
前列腺根治性切除术后控尿功能恢复的预测模型可以在术前评估患者尿失禁的发生风险，有助于为前列腺癌患者选择恰当的治疗方法。既往研究中，术后控尿功能恢复的预测模型主要基于患者的临床因素和问卷调查结果构建[8-10]。本研究通过回顾性分析2016年1月至2020年1月于北京大学第三医院行腹腔镜根治性前列腺切除术(laparoscopic radical prostatectomy，LRP)的前列腺癌患者术后控尿功能恢复情况，探讨基于MRI测量的腺体相关参数构建预测LRP术后尿失禁的预测模型。
1. 资料与方法
1.1. 临床资料
回顾性分析2016年1月至2020年1月于北京大学第三医院经前列腺穿刺活检诊断为前列腺腺癌并接受LRP手术的患者，排除标准为既往前列腺手术史或尿失禁病史、术前未行MRI检查、术前因尿潴留留置尿管、已行新辅助内分泌治疗或放疗，临床资料不齐备等。收集患者的临床资料，包括年龄、体重指数(body mass index，BMI)、前列腺特异性抗原(prostate specific antigen，PSA)、穿刺Gleason评分、临床分期等，共纳入满足条件的患者202例。
1.2. MRI检查方法及数据测量
所有患者术前MRI检查于前列腺穿刺活检术前1周内完成，使用西门子3.0T超导磁共振检测仪，应用腹部相控阵线圈接受信号。扫描包含前列腺和两侧精囊腺，常规行轴位、矢状位和冠状位快速自旋回波T2WI和轴位T1WI。冠状位MRI检查测量MUL，将MUL定义为前列腺尖部尿道至进入阴茎球部尿道之间的距离。MRI腺体相关参数包含前列腺上下径、左右径、前后径、前列腺体积、IPPL、前列腺尖部形态分型等。前列腺体积的测量公式为0.52×上下径×前后径×左右径，IPPL定义为矢状位测量突入膀胱的前列腺组织顶点至膀胱基底部的垂直距离。根据MRI将前列腺尖部形态定义为四型(Lee分型)[11]：A型为前列腺尖部腺体覆盖前方和后方膜性尿道；B型为前列腺尖部腺体覆盖前方膜性尿道；C型为前列腺尖部腺体覆盖后方膜性尿道；D型为前列腺尖部腺体未覆盖前方和后方膜性尿道。
1.3. 手术方法
麻醉完成后，患者取仰卧位，腰部垫高，头低脚高位。于脐下切口置入穿刺器建立气腹，并于左侧腹直肌外缘、右侧腹直肌外缘和右侧髂前上嵴内侧放置3个穿刺器；分离膀胱前壁及两侧壁疏松组织，显露前列腺腹侧并分离暴露盆筋膜；剪开盆筋膜后紧贴前列腺沿前列腺边缘游离至前列腺尖部，缝扎阴茎背深静脉复合体；沿膀胱颈前列腺交界处切开膀胱颈前壁，拔除尿管，腹壁悬吊尿管以抬高前列腺底部，紧贴前列腺打开膀胱颈后壁，使前列腺与膀胱分离；暴露双侧输精管并切断，分离精囊；在两侧精囊之间剪开狄氏筋膜(Denonvillier fascia)，分离狄氏筋膜至前列腺尖部。对于术前评估及术中探查可保留神经血管束的患者，在前列腺侧后方用剪刀沿前列腺包膜锐性分离出神经血管束并予保留。钝性分离前列腺尖部的尿道并尽量保留膜性尿道，剪断尿道将前列腺完整切除。必要时重建膀胱颈口，膀胱尿道吻合采取5/8弧单针连续吻合，吻合后留置尿管。
1.4. 术后控尿功能评价
自术后第1个月起，每个月均对患者控尿功能恢复情况进行随访，依照以下评价标准：控尿为患者全天无漏尿，不需要使用尿垫；尿失禁为患者每日需使用≥1个尿垫。
1.5. 统计学方法
采用R 4.0.3统计软件进行统计分析。将数据集按照7 ∶3的比例随机分为训练集和验证集，训练集的样本量为141，验证集的样本量为61。连续变量使用Shapiro正态性检验判定样本数据的正态性，如果符合正态分布，采用均值±标准差表示，两组间比较采用t检验；如果不符合正态分布，采用中位数(P25，P75)表示，两组间比较采用Wilcox检验。分类数据采用频数(百分比)进行统计描述，组间比较采用χ2检验或Fisher’s精确检验，双侧P < 0.05认为差异有统计学意义。
使用训练集的数据，应用lrm函数进行二元Logistic回归分析，自变量为分类变量时，以最小值组作为参照组；自变量为连续变量时，直接将连续变量纳入二元Logistic回归模型。变量筛选采用后退法，根据Logistic回归结果绘制预测模型的受试者操作特征(receiver operator characteristic，ROC)曲线，报告区分度和校准度，并在验证集中分析预测模型的表现。以决策曲线分析(decision curve analysis，DCA)评价模型的临床净获益，并绘制预测模型的列线图以供临床使用。
2. 结果
本研究共纳入202例患者，平均年龄为69.0(64.0, 75.5)岁，平均穿刺前PSA为12.12 (7.36, 20.06) μg/L，穿刺Gleason评分 < 7分和≥7分者分别为73例(36.2%)和129例(63.9%)，临床分期为T1/T2期者100例(49.5%)，T3期者102例(50.5%)。经术前MRI测量，前列腺体积为35.4 (26.2, 51.1) mL，前列腺上下径与左右径的比值为0.91(0.77, 1.07)，MUL为15 (11, 16) mm，IPPL为2 (0, 6) mm，前列腺尖部形态分型A~D型分别为67例(33.2%)、80例(39.6%)、24例(11.9%)和31例(15.3%)，训练集和验证集分别为141例和61例，患者基线情况如表 1所示。
表 1.
训练集和验证集患者基线的比较
Comparison of patients characteristics between training dataset and validation dataset
| Items | All patients (n=202) |
Training dataset (n=141) |
Validation dataset (n=61) |
| PSA, prostate specific antigen; cT, clinical stage; PV, prostatic volume; MUL, membranous urethral length; IPPL, intravesical prostatic protrusion length. | |||
| Age/years, n (%) | |||
| ≥70 | 109 (54.0) | 77 (54.6) | 32 (52.5) |
| < 70 | 93 (46.0) | 64 (45.4) | 29 (47.5) |
| Pre-biopsy PSA/(μg/L), M (P25, P75) | 12.12 (7.36, 20.06) | 10.98 (7.43, 19.31) | 12.90 (7.10, 21.80) |
| Biopsy Gleason score, n (%) | |||
| ＜7 | 73 (36.1) | 56 (39.7) | 17 (27.9) |
| ≥7 | 129 (63.9) | 85 (60.3) | 44 (72.1) |
| cT, n (%) | |||
| T1/T2 | 100 (49.5) | 66 (46.8) | 34 (55.7) |
| T3 | 102 (50.5) | 75 (53.2) | 27 (44.3) |
| PV/mL, M (P25, P75) | 35.4 (26.2, 51.1) | 35.8 (27.1, 50.5) | 33.9 (23.4, 53.7) |
| MUL/mm, M (P25, P75) | 15 (11, 16) | 15 (11, 16) | 15 (11, 17) |
| IPPL/mm, M (P25, P75) | 2 (0, 6) | 2 (0, 6) | 2 (0, 8) |
| Length/width, M (P25, P75) | 0.91 (0.77, 1.07) | 0.91 (0.82, 1.07) | 0.89 (0.74, 1.06) |
| Prostate apex shape, n (%) | |||
| A-C | 171 (84.7) | 122 (86.5) | 49 (80.3) |
| D | 31 (15.3) | 19 (13.5) | 12 (19.7) |
所有患者手术均顺利完成，随访3个月患者的控尿率为59.4%(120/202例)。在训练集术后早期(3个月)尿失禁的单因素分析中，患者年龄、穿刺前PSA、穿刺Gleason评分差异均无统计学意义(P>0.05)，而临床分期(P=0.014)、前列腺体积(P=0.005)、MUL(P < 0.001)、IPPL(P < 0.001)和上下径/左右径的比值(P=0.012)差异有统计学意义并进入多因素分析，前列腺尖部形态分型(P=0.056)虽然差异无统计学意义，但也进入了多因素分析(表 2)。
表 2.
训练集术后3个月尿失禁的单因素分析
Univariate analysis of continence recovery 3 months of training dataset after surgery
| Items | Continence (n=58) |
Incontinence (n=83) |
t/χ2/z value | P value |
| Abbreviations as in Table 1. | ||||
| Age/years, n (%) | 1.595 | 0.207 | ||
| ≥70 | 28 (48.3) | 49 (59.0) | ||
| < 70 | 30 (51.7) | 34 (41.0) | ||
| Pre-biopsy PSA/(μg/L), M (P25, P75) | 13.59 (7.62, 22.31) | 10.27 (7.16, 17.15) | 0.953 | 0.340 |
| Biopsy Gleason score, n (%) | 0.114 | 0.736 | ||
| ＜7 | 24 (41.4) | 32 (38.6) | ||
| ≥7 | 34 (58.6) | 51 (61.4) | ||
| cT, n (%) | 6.012 | 0.014 | ||
| T1/T2 | 20 (34.5) | 46 (55.4) | ||
| T3 | 38 (65.5) | 37 (44.6) | ||
| PV/mL, M (P25, P75) | 41.51 (31.49, 56.42) | 34.53 (23.7, 44.33) | 2.786 | 0.005 |
| MUL/mm, M (P25, P75) | 11 (9, 14) | 15 (14, 17) | -6.059 | < 0.001 |
| IPPL/mm, M (P25, P75) | 6 (0, 10) | 0 (0, 3) | 4.788 | < 0.001 |
| Prostate apex shape, n (%) | 3.657 | 0.056 | ||
| A-C | 54 (93.1) | 68 (81.9) | ||
| D | 4 (6.9) | 15 (18.1) | ||
| Length/width, M (P25, P75) | 0.99 (0.85, 1.13) | 0.88 (0.77, 1.01) | 2.506 | 0.012 |
多因素分析结果显示，MUL(P < 0.001)、IPPL(P=0.017)和临床分期(P=0.022)是术后早期(3个月)尿失禁发生的独立危险因素(表 3)。
表 3.
术后3个月患者控尿功能恢复的临床多因素分析
Multivariate analysis of continence recovery 3 months
| Items | B | S.E. | z | P | OR (95%CI) |
| Abbreviations as in Table 1. | |||||
| IPPL | -0.140 | 0.059 | -2.384 | 0.017 | 0.87 (0.78, 0.98) |
| MUL | 0.367 | 0.073 | 5.021 | < 0.001 | 1.44 (1.25, 1.67) |
| cT | -1.086 | 0.475 | -2.286 | 0.022 | 0.34 (0.13, 0.86) |
| Length/width | -2.476 | 1.269 | -1.950 | 0.051 | 0.08 (0.01, 1.01) |
| Constant | -0.143 | 1.597 | -0.089 | 0.929 | |
根据多因素分析结果制作列线图和临床决策曲线。应用验证集的数据绘制校准曲线，使用pROC绘制ROC曲线，计算训练集ROC曲线下面积(area under the curve, AUC)值为0.885 (0.826, 0.944)，验证集AUC值为0.854 (0.757, 0.950)。在验证集里对模型进行Hosmer-Lemeshow拟合优度检验，卡方值为5.426 (P=0.711)，见图 1~3。
图 1.
训练集(A)和验证集(B)预测LRP术后早期控尿功能恢复的ROC曲线
ROC curves of continence recovery after LRP of training dataset (A) and validation dataset (B)
图 3.
预测LRP术后早期控尿功能恢复的列线图(A)和DCA图(B)
The nomogram (A) and DCA (B) of continence recovery after LRP of training dataset and validation dataset
图 2.
训练集(A)和验证集(B)预测LRP术后早期控尿功能恢复的校正曲线
Calibration plot of continence recovery after LRP of training dataset (A) and validation dataset (B)
3. 讨论
尿失禁是前列腺根治性切除术后最常见的并发症之一，其发生机制与手术损伤尿道外括约肌及其支配神经、影响血液供应和术后不稳定膀胱有关[12]。盆腔MRI检查可在前列腺根治性切除术前深入了解前列腺癌患者膀胱、前列腺、后尿道及其周围结构，既往研究证实，盆腔MRI检查提示的解剖学参数与术后控尿功能恢复存在相关性。前列腺腺体的大小、形状及其与膀胱之间的关系对前列腺根治性切除术中的多个手术环节造成影响，巨大体积前列腺和中叶突入膀胱的患者围手术期并发症发生的风险增加，控尿功能延迟恢复。前列腺尖部形状的分型最早由Lee等[11]提出，根据前列腺尖部腺体覆盖尿道的部位进行分型(A~D型)，不同分型的患者术后控尿功能恢复存在差异。本研究通过对202例接受LRP手术患者的临床影像资料及术后控尿功能恢复情况进行分析，特别是基于MRI检查腺体相关参数的结果，构建了预测术后控尿功能恢复的统计学模型。
本研究中，临床分期、MUL和IPPL均为LRP术后3个月控尿功能恢复的独立危险因素。MUL的定义为前列腺尖部尿道至进入海绵体部尿道的距离，已有多项临床研究和荟萃分析证实，术前MUL较短是前列腺根治性切除术后尿失禁的独立危险因素[7, 13]。在不影响去除肿瘤的前提下，术中应尽量保留MUL，保存功能性尿道长度是改善术后控尿功能恢复的关键[14-15]。对于术前MUL较短的患者，术前应充分告知术后控尿功能延迟恢复的风险，术中膀胱颈重建等技术改进能够部分弥补较短MUL对于控尿功能恢复的负面影响。
前列腺体积是最为常用的与围手术期预后和功能性预后相关的腺体参数，较大体积的前列腺对于保留神经血管束、保留功能性尿道长度及膀胱尿道吻合均存在负面影响。不同形态的前列腺同样会影响LRP的手术进程，本组患者的手术均由膀胱前入路完成，前列腺上下径与左右径的比值可反映前列腺的形状，单因素分析中，两组间此比值存在统计学意义，但在多因素分析中，此比值未达到早期控尿功能恢复的独立危险因素，其可能的原因为前列腺上下径大于左右径者，由于视野遮挡，不利于保留尖部周围与控尿功能的相关结构及MUL，特别是对于窄骨盆的前列腺癌患者。前列腺突入膀胱是LRP术中面临的困难局面[16]，通过术前MRI测量IPPL可量化评估前列腺突入膀胱的程度。既往研究提示，术前IPPL≥5 mm的患者术后控尿功能延迟恢复[17]，与本研究结果相符。本研究考虑到样本量因素，将患者按Lee分型分为前列腺尖部腺体覆盖尿道组(A~C型)和未覆盖尿道组(D型)，两组在单因素分析中无统计学意义，故未纳入统计模型。Lee分型在预测术后控尿功能恢复的价值尚未明确，我们应准确辨认前列腺尖部解剖结构，MRI测量的较短MUL仍然是LRP术后尿失禁最为可靠的危险因素之一[18]。
相比于既往的预测前列腺根治性切除术后控尿功能恢复的列线图，本研究将术前MRI提示的腺体相关参数引入预测模型，更准确地评估了术后尿失禁发生风险。构建基于腺体相关参数预测LRP术后控尿功能恢复的模型，可用于前列腺癌手术的术前咨询和患者教育，同时，利用此模型我们还可以识别前列腺癌患者术后尿失禁的发生风险，并据此进行术中技术的改进和术后的功能康复。
本研究的局限性主要有：(1)本研究是基于回顾性、单中心、非单一术者的临床资料构建的统计学模型且缺乏外部验证，有可能影响研究的可靠性；(2)不同手术技术的迭代可能影响前列腺根治性切除术后控尿功能恢复危险因素的判断；(3)客观的尿动力学检查能够更为深入地评估术后尿失禁的发生机制以及控尿功能恢复与解剖学参数之间的关系，但本研究缺乏尿动力学的数据，这也是我们下一步工作的方向。
综上所述，术前MUL、IPPL、临床分期是LRP术后早期尿失禁发生的独立危险因素，基于MRI腺体相关参数构建的列线图可有效预测LRP术后早期控尿功能恢复，此研究结果还需要更大规模的临床研究证实。
Contributor Information
黄 毅 (Yi HUANG), Email: pku_huang@163.com.
褚 红玲 (Hong-ling CHU), Email: 18810530974@163.com.
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