腹腔镜直肠癌根治术中肠系膜下动脉低位结扎对第3站淋巴结清扫的影响及第3站淋巴结转移危险因素分析

Effects and risk factors of low ligation of the inferior mesenteric artery on the third station lymph node dissection and metastasis in laparoscopic radical resection of rectal cancer

目的：探讨腹腔镜直肠癌根治术中肠系膜下动脉（IMA）低位结扎对第3站淋巴结清扫的影响，分析影响直肠癌第3站淋巴结转移的危险因素。方法：采用回顾性队列研究方法。收集2014年6月至2016年6月上海交通大学医学院附属仁济医院收治的380例直肠癌患者的临床资料。380例患者中，177例术中保留左结肠动脉，设为IMA低位结扎组，203例术中不保留左结肠动脉，设为IMA高位结扎组。患者均按全直肠系膜切除术原则行腹腔镜直肠癌根治术。观察指标：（1）术中及术后恢复情况。（2）术后病理学检查结果。（3）随访和生存情况。（4）影响直肠癌第3站淋巴结转移的危险因素分析。采用门诊、电话方式进行术后随访，了解患者术后无病生存情况和肿瘤复发、转移情况。随访时间截至2017年5月31日。正态分布的计量资料以±s表示，组间比较采用t检验。计数资料比较采用X2检验。等级资料比较采用U检验。采用KaplanMeier法计算生存率并绘制生存曲线，采用Logrank检验进行生存分析。结果：（1）术中及术后恢复情况：两组患者均顺利完成手术。IMA低位结扎组和IMA高位结扎组患者手术时间、术后首次肛门排气时间、吻合口瘘分别为（147.2±3.0）min和（137.2±2.8）min、（72.8±1.4）h和（76.6±1.1）h、 20例和38例，两组患者上述指标比较，差异均有统计学意义（t=2.463，2.073， X2=4.025，P〈0.05）。IMA低位结扎组和IMA高位结扎组直肠癌患者术中出血量分别为（119±6）mL和（108±5）mL、预防性造瘘分别为25例和32例、血管损伤（肠系膜下血管以及骶前静脉损伤）分别为29例和27例、尿潴留分别为24例和30例、术后住院时间分别为（10.7± 0.5）d和（9.6±0.4）d，两组患者上述指标比较，差异均无统计学意义（t=1.524， X2=0.235，0.716，1.115，t=1.780，P〉0.05）。58例术后发生吻合口瘘患者中， 31例预先行末端回肠襻式造口术，13例给予保守治疗，14例术后给予末端回肠襻式造口术。54例术后发生尿潴留患者，给予留置导尿管。所有并发症患者治疗后好转，顺利出院。（2）术后病理学检查结果：IMA低位结扎组和IMA高位结扎组患者淋巴结清扫数目分别为（12.8±0.4）枚和（12.0±0.3）枚，肿瘤侵犯肠壁深度（pT1～T2、pT3～T4期）分别为53、124例和59、144例，肿瘤组织病理学类型（管状腺癌、非管状腺癌）分别为150、27例和176、27例，肿瘤分化程度（高分化、中分化、低分化）分别为81、63、33例和99、59、 45例，淋巴结转移程度（N0、N1、N2期）分别为73、66、38例和79、78、46例，第3站淋巴结转移（有、无）分别为16、161例和24、179例，TNM分期（Ⅰ、Ⅱ、Ⅲ、Ⅳ期）分别为17、54、93、13例和32、47、105、19例，两组患者上述指标比较，差异均无统计学意义（t=1.556， X2=0.035，0.296，U=2.002， 0.220， X2=0.778，U=5.557，P〉0.05）。（3）随访和生存情况：380例患者中338例获得随访，其中IMA低位结扎组164例，IMA高位结扎组174例。随访时间为6～36个月，平均随访时间为28个月。IMA低位结扎组患者1、3年无病生存率分别为93.9%、76.4%，39例术后发生肿瘤复发转移；IMA高位结扎组患者1、3年无病生存率分别为94.8%、79.3%，36例术后发生肿瘤复发转移，两组患者生存情况比较，差异无统计学意义（X2=0.861， P〉0.05）。（4）影响直肠癌第3站淋巴结转移的危险因素分析：单因素分析结果显示：肿瘤部位、肿瘤直径、肿瘤侵犯肠壁深度、肿瘤组织病理学类型是影响直肠癌患者第3站淋巴结转移的相关因素（X2=9.957，9.921，6.196，6.576，P〈0.05）。多因素分析结果显示：肿瘤直径〉5 cm和肿瘤组织病理学类型为非管状腺癌是影响直肠癌患者第3站淋巴结转移的独立危险因素（比值比=2.561，2.296，95%可信区间：1.280～5.123，1.037～5.083，P〈0.05）。结论：腹腔镜直肠癌根治术中IMA低位结扎安全可行，可达到与IMA高位结扎同样彻底的淋巴结清扫效果，且不影响第3站淋巴结清扫和患者短期无病生存率。肿瘤直径〉5 cm和肿瘤组织病理学类型为非管状腺癌是影响直肠癌第3站淋巴结转移的独立危险因素。

Objective：To explore the effects of low ligation of the inferior mesenteric artery （IMA） on the third station lymph node dissection in laparoscopic radical resection of rectal cancer （RC）, and analyze the risk factors affecting the third station lymph node metastasis. Methods：The retrospective cohort study was conducted. The clinical data of 380 RC patients who were admitted to Renji Hospital of Shanghai Jiaotong University School of Medicine from June 2014 to June 2016 were collected. Of 380 patients, 177 with preservation of left colic artery （LCA） and 203 without preservation of LCA were respectively allocated into the low ligation group and high ligation group. All the patients received laparoscopic radical resection of RC based on the principle of total mesorectal excision （TME）. Observation indicators： （1） intra and postoperative recovery situations; （2） results of postoperative pathological examination; （3） followup and survival; （4） risk factors analysis affecting the third station lymph node metastasis. Followup using outpatient examination and telephone interview was performed to detect postoperative diseasefree survival and tumor recurrence or metastasis up to May 31, 2017. Measurement data with normal distribution were represented as ±s, and comparisons between groups were evaluated with the t test. Comparisons of count data and ordinal data were respectively analyzed using the chisquare test and U test. The survival curve and survival rate were respectively drawn and analyzed using the KaplanMeier method, and the survival analysis was done by the Logrank test. Results：（1） Intra and postoperative recovery situations： all the patients underwent successful surgery. The operation time, time to initial exsufflation and cases with anastomotic leakage were respectively （147.2±3.0）minutes, （72.8± 1.4）hours, 20 in the low ligation group and （137.2±2.8）minutes, （76.6±1.1）hours, 38 in the high ligation group, with statistically significant differences between groups （t=2.463, 2.073, X2=4.025, P〈0.05）. Volume of intraoperative blood loss, cases with temporary stoma, vascular injury （injury of inferior mesenteric vessels and presacral vein injury）, urinary retention and duration of postoperative hospital stay were respectively （119±6）mL, 25, 29, 24, （10.7± 0.5）days in the low ligation group and （108±5）mL, 32, 27, 30, （9.6±0.4）days in the high ligation group, with no statistically significant difference between groups （t=1.524, X2=0.235, 0.716, 1.115, t=1.780, P〉0.05）. Of 58 patients with anastomotic leakage, 31 received previously terminal loop ileostomy, 13 received conservative treatment and 14 received postoperatively terminal loop ileostomy. Fiftyfour patients with urinary retention received urethral catheterization. All the patients with complications were improved by treatment and then were discharged. （2） Results of postoperative pathological examination： number of lymph node dissected in the low ligation group and high ligation group was respectively 12.8±0.4 and 12.0±0.3; cases with depths of tumor invading to intestinal wall in stage pT1T2 and pT3T4, with tubular adenocarcinoma and nontubular adenocarcinoma, with highdifferentiated, moderatedifferentiated and lowdifferentiated tumors, with lymph node metastasis in stage N0, N1 and N2, with and without the third station lymph node metastasis, with TNM staging in stage Ⅰ, Ⅱ, Ⅲ, and Ⅳ were respectively 53, 124, 150, 27, 81, 63, 33, 73, 66, 38, 16, 161, 17, 54, 93, 13 in the low ligation group and 59, 144, 176, 27, 99, 59, 45, 79, 78, 46, 24, 179, 32, 47, 105, 19 in the high ligation group, with no statistically significant difference in above indicators between groups （t=1.556, X2=0.035, 0.296, U=2.002, 0.220, X2=0.778, U=5.557, P〉0.05）. （3） Followup and survival： 338 of 380 patients were followed up for 6-36 months, with an average time of 28 months, including 164 in the low ligation group and 174 in the high ligation group. The 1 and 3year diseasefree survival rates and cases with postoperative tumor recurrence or metastasis were respectively 93.9%, 76.4%, 39 in the low ligation group and 94.8%, 79.3%, 36 in the high ligation group, with no statistically significant difference between groups （X2=0.861, P〉0.05）. （4） Risk factors analysis affecting the third station lymph node metastasis： results of univariate analysis showed that tumor location and diameter, depth of tumor invading to intestinal wall and tumor histopathological type were related factors affecting the third station lymph node metastasis of RC patients （X2=9.957, 9.921, 6.196, 6.576, P〈0.05）. Results of multivariate analysis showed that tumor diameter 〉 5 cm and nontubular adenocarcinoma were independent risk factors affecting the third station lymph node metastasis of RC patients （Odds ratio=2.561, 2.296, 95% confidence interval： 1.280-5.123, 1.037-5.083, P〈0.05）. Conclusions：The low ligation of the IMA is safe and feasible in laparoscopic radical resection of RC, meanwhile, it has the same radical effect in lymph node dissection and doesn′t affect the third station lymph node metastasis and shortterm diseasefree survival compared with high ligation of the IMA. Tumor diameter 〉5 cm and nontubular adenocarcinoma are independent risk factors affecting the third station lymph node metastasis of RC.