陳俊強(qiáng)鄭雄偉朱坤壽李建成林宇潘才住潘建基

1. 福建醫(yī)科大學(xué)教學(xué)醫(yī)院，福建省腫瘤醫(yī)院放療科，福建 福州350014；

2. 福建醫(yī)科大學(xué)教學(xué)醫(yī)院，福建省腫瘤醫(yī)院病理科，福建 福州350014；

3. 福建醫(yī)科大學(xué)教學(xué)醫(yī)院，福建省腫瘤醫(yī)院胸外科，福建 福州350014

胸段食管鱗癌頸部淋巴結(jié)轉(zhuǎn)移特點(diǎn)及其臨床意義

陳俊強(qiáng)1鄭雄偉2朱坤壽3李建成1林宇1潘才住1潘建基1

1. 福建醫(yī)科大學(xué)教學(xué)醫(yī)院，福建省腫瘤醫(yī)院放療科，福建 福州350014；

2. 福建醫(yī)科大學(xué)教學(xué)醫(yī)院，福建省腫瘤醫(yī)院病理科，福建 福州350014；

3. 福建醫(yī)科大學(xué)教學(xué)醫(yī)院，福建省腫瘤醫(yī)院胸外科，福建 福州350014

背景與目的：食管癌頸部淋巴結(jié)轉(zhuǎn)移率較高，但少有專門報(bào)道。本研究分析胸段食管鱗癌頸部淋巴結(jié)轉(zhuǎn)移特點(diǎn)，探討其臨床意義。方法：選擇1993年1月—2003年12月在福建省腫瘤醫(yī)院行胸段食管鱗癌三野淋巴結(jié)清掃根治術(shù)患者1 131例，對(duì)術(shù)后病理證實(shí)頸部淋巴結(jié)轉(zhuǎn)移患者376例的具體情況進(jìn)行分析。結(jié)果：全組頸部淋巴結(jié)轉(zhuǎn)移率為33.2%，其中胸上、中及下段的頸部淋巴結(jié)轉(zhuǎn)移率分別為43.7%、33.0%和16.0%。單因素分析顯示，頸部淋巴結(jié)轉(zhuǎn)移率與腫瘤部位、病理分化程度、病變X線長(zhǎng)度、pT分期以及淋巴結(jié)轉(zhuǎn)移個(gè)數(shù)有關(guān)(P＜0.05)，但多因素回歸分析顯示，頸部淋巴結(jié)轉(zhuǎn)移率只與腫瘤部位、pT分期及淋巴結(jié)轉(zhuǎn)移個(gè)數(shù)有關(guān)(P＜0.05)。頸段食管旁淋巴結(jié)轉(zhuǎn)移最多見(jiàn)，其次是鎖骨上淋巴結(jié)轉(zhuǎn)移，頸深淋巴結(jié)及咽后淋巴結(jié)轉(zhuǎn)移少見(jiàn)；胸上、中及下段的頸部淋巴結(jié)轉(zhuǎn)移數(shù)占該段淋巴結(jié)總轉(zhuǎn)移數(shù)的比率分別為57.7%、32.0%和10.0%，差異有統(tǒng)計(jì)學(xué)意義(P＜0.05)；各段食管癌右頸部淋巴結(jié)轉(zhuǎn)移多于左頸部。結(jié)論：影響胸段食管鱗癌頸部淋巴結(jié)轉(zhuǎn)移獨(dú)立因素是腫瘤部位、pT分期及淋巴結(jié)轉(zhuǎn)移數(shù)；頸段食管旁淋巴結(jié)轉(zhuǎn)移最多見(jiàn)，其次是鎖骨上淋巴結(jié)轉(zhuǎn)移，頸深淋巴結(jié)及咽后淋巴結(jié)轉(zhuǎn)移少見(jiàn)。

食管腫瘤；頸部淋巴結(jié)轉(zhuǎn)移；淋巴結(jié)轉(zhuǎn)移數(shù)；淋巴結(jié)轉(zhuǎn)移率

淋巴結(jié)轉(zhuǎn)移是食管癌最常見(jiàn)的轉(zhuǎn)移途徑，特別是頸部具有較高的轉(zhuǎn)移率(23.4%～49.5%)［1-4］。近20年來(lái)隨著外科進(jìn)展，下頸、右胸、上腹三野淋巴結(jié)清掃的食管癌根治術(shù)成為胸段食管癌的主要治療手段，該術(shù)式手術(shù)暴露好，淋巴結(jié)清掃徹底，能夠較為真實(shí)體現(xiàn)淋巴結(jié)轉(zhuǎn)移情況［1,5］。目前有關(guān)胸段食管鱗癌頸部淋巴結(jié)轉(zhuǎn)移特點(diǎn)少有專門報(bào)道，本研究對(duì)1 131例胸段食管鱗癌三野淋巴結(jié)清掃根治術(shù)中有頸部淋巴結(jié)轉(zhuǎn)移的376例進(jìn)行回顧性分析，結(jié)果報(bào)道如下。

1 資料和方法

1.1 病例選擇

入組條件：①須福建省腫瘤醫(yī)院收治的首程治療行頸部、右胸部、上腹部三野淋巴結(jié)清掃的胸段食管癌根治術(shù)，且清除淋巴結(jié)總數(shù)≥15個(gè)；②術(shù)前體檢雙頸及鎖骨上區(qū)未捫及腫大淋巴結(jié)；③未行術(shù)前放療或化療；④術(shù)后病理診斷為鱗癌，無(wú)遠(yuǎn)處臟器轉(zhuǎn)移。

1.2 手術(shù)方法

經(jīng)右胸后外側(cè)切口、上腹正中切口、下頸部U字形切口行全胸段食管合并賁門及部分小彎切除，大彎側(cè)胃管經(jīng)食管床于頸部與食管行吻合術(shù)，清除雙下頸鎖骨上、縱隔、上腹部引流區(qū)淋巴結(jié)，以右喉返神經(jīng)起始部為界劃分頸部淋巴結(jié)和縱隔淋巴結(jié)［1］。根據(jù)日本食管疾病淋巴結(jié)分組標(biāo)準(zhǔn)［6］，頸部淋巴結(jié)包括101(頸段食管旁淋巴結(jié))、102(下頸深淋巴結(jié))、103(咽后淋巴結(jié))、104(鎖骨上淋巴結(jié))，左、右側(cè)分別用R、L表示。

1.3 統(tǒng)計(jì)學(xué)處理

應(yīng)用SPSS 15.0統(tǒng)計(jì)軟件分析資料，定量資料組間比較采用方差檢驗(yàn)，定性資料組間比較采用χ2檢驗(yàn)，多因素采用Logistic回歸分析。P＜0.05為差異有統(tǒng)計(jì)學(xué)意義。

2 結(jié) 果

2.1 各段食管癌鎖骨上區(qū)域淋巴結(jié)轉(zhuǎn)移特點(diǎn)

1993年1月—2003年12月符合入組條件患者共1 131例，術(shù)后病理證實(shí)有頸部淋巴結(jié)轉(zhuǎn)移376例。全組共清除淋巴結(jié)28 227枚，平均每例清除淋巴結(jié)25.0枚(15～73枚)，淋巴結(jié)陽(yáng)性總數(shù)2 418枚，總轉(zhuǎn)移度為8.6，其中胸上段、胸中段及胸下段的淋巴結(jié)轉(zhuǎn)移度分別為6.9、8.9和8.9；各段淋巴結(jié)總清除數(shù)及淋巴結(jié)轉(zhuǎn)移總數(shù)差異無(wú)統(tǒng)計(jì)學(xué)意義(P＞0.05)，但各段在頸部、縱隔及腹部淋巴結(jié)轉(zhuǎn)移數(shù)差異有統(tǒng)計(jì)學(xué)意義(P＜0.05)，其中胸上段、胸中段及胸下段的頸部淋巴結(jié)轉(zhuǎn)移數(shù)在該段所占比率分別為57.7%、32.0%和10.0%，差異有統(tǒng)計(jì)學(xué)意義(P＜0.05，表1)。

表 1 1 131例胸段食管癌各段淋巴結(jié)轉(zhuǎn)移特點(diǎn)比較Tab. 1 Characteristics of 1 131 patients with TE-SCC

全組頸部淋巴結(jié)轉(zhuǎn)移率為33.2%，其中胸上段、胸中段及胸下段的頸部淋巴結(jié)轉(zhuǎn)移率分別為43.7%、33.0%和16.0%(P＜0.000 1)，術(shù)后(pT)分期的T1、T2、T3及T4頸部淋巴結(jié)轉(zhuǎn)移率分別為18.6%、29.1%、34.5%和42.2%。各段在101L組、101R組和104R淋巴結(jié)轉(zhuǎn)移率差異有統(tǒng)計(jì)學(xué)意義(P＜0.05，表2)。

2.2 頸部淋巴結(jié)轉(zhuǎn)移率與臨床因素關(guān)系

單因素分析顯示，頸部淋巴結(jié)轉(zhuǎn)移率與腫瘤部位、病理分化程度、病變X線長(zhǎng)度、pT分期以及淋巴結(jié)轉(zhuǎn)移數(shù)差異有統(tǒng)計(jì)學(xué)意義(P＜0.05)，與性別及年齡差異無(wú)統(tǒng)計(jì)學(xué)意義(P＞0.05，表3)。但多變量Logistic回歸分析顯示，頸部淋巴結(jié)轉(zhuǎn)移率只與腫瘤部位、pT分期及淋巴結(jié)轉(zhuǎn)移數(shù)有關(guān)(P＜0.000 1，表4)。

表 2 367例頸部淋巴結(jié)陽(yáng)性具體部位轉(zhuǎn)移率[例(%)]Tab. 2 Number of cervical lymph node metastasis in 367 patients

表 3 頸部淋巴結(jié)轉(zhuǎn)移率與臨床因素關(guān)系單因素分析Tab. 3 Univariate analysis of prognostic factors of cervical LNM

表 4 頸部淋巴結(jié)轉(zhuǎn)移與臨床因素關(guān)系多因素Logistic回歸分析Tab. 4 Multiple logistic regression analysis of prognostic factors of cervical LNM

3 討 論

食管癌是我國(guó)最常見(jiàn)的惡性腫瘤之一，死亡率位居第4位，食管鱗癌是主要的病理類型，占95%以上，且絕大多數(shù)發(fā)生于胸段食管［7］。由于胸段食管癌淋巴結(jié)轉(zhuǎn)移具有明顯的上下雙向轉(zhuǎn)移和跳躍性轉(zhuǎn)移特點(diǎn)，特別是頸部具有較高的淋巴結(jié)轉(zhuǎn)移率［1］。目前對(duì)于手術(shù)是否要進(jìn)行頸部淋巴結(jié)清掃，放療是否要包括頸部淋巴結(jié)引流區(qū)預(yù)防照射，國(guó)內(nèi)外學(xué)者仍存在爭(zhēng)議，尚無(wú)共識(shí)。2009年公布的第7版AJCC食管癌分期中將淋巴結(jié)轉(zhuǎn)移個(gè)數(shù)作為N分期的標(biāo)準(zhǔn)［8］，了解胸段食管鱗癌頸部淋巴結(jié)轉(zhuǎn)移特點(diǎn)，對(duì)指導(dǎo)食管癌分期、放療靶區(qū)的設(shè)計(jì)以及手術(shù)方式有非常重要的臨床意義。

頸部是早、晚期食管癌常見(jiàn)的淋巴結(jié)轉(zhuǎn)移部位，Igaki等［9］報(bào)道黏膜下浸潤(rùn)的胸段食管癌頸部淋巴結(jié)轉(zhuǎn)移率高達(dá)17%；Koide等［10］報(bào)道T2或T3的胸中段食管癌頸部淋巴結(jié)轉(zhuǎn)移率為27.4%；本研究T1、T2、T3及T4的胸段食管癌頸部淋巴結(jié)轉(zhuǎn)移率分別為18.6%、29.1%、34.5%和42.2%。腫瘤部位是食管癌頸部淋巴結(jié)轉(zhuǎn)移最主要因素，Akiyama等［2］報(bào)道290例食管癌三野淋巴結(jié)清掃根治術(shù)，總頸部淋巴結(jié)轉(zhuǎn)移率為31.0%，其中胸上段、中段及下段分別為46.3%、29.2%和27.2%；Ando等［3］報(bào)道116例食管癌三野淋巴結(jié)清掃根治術(shù)，總頸部淋巴結(jié)轉(zhuǎn)移率為28.0%，胸上段、中段及下段分別為39.0%、26.0%和24.0%。本研究總頸部淋巴結(jié)轉(zhuǎn)移率為33.2%，胸上段、中段及下段的頸部淋巴結(jié)轉(zhuǎn)移率分別為43.7%、33.0%和16.0%(P＜0.000 1)，與文獻(xiàn)報(bào)道的數(shù)據(jù)大致相同［2-3］。

縱隔喉返神經(jīng)旁淋巴結(jié)轉(zhuǎn)移與頸部淋巴結(jié)轉(zhuǎn)移有明顯相關(guān)性，Shimada等［11］報(bào)道喉返神經(jīng)旁淋巴結(jié)轉(zhuǎn)移是頸淋巴結(jié)轉(zhuǎn)移與否的獨(dú)立預(yù)測(cè)因子。Tabira等［12］報(bào)道喉返神經(jīng)旁淋巴結(jié)有無(wú)轉(zhuǎn)移其頸部淋巴結(jié)轉(zhuǎn)移率分別為43.5%和11.1%；Yoshioka等［13］也報(bào)道有無(wú)喉返神經(jīng)旁淋巴結(jié)轉(zhuǎn)移者的頸部淋巴結(jié)轉(zhuǎn)移率分別為51.6%和11.6%。本研究單因素分析顯示，頸部淋巴結(jié)轉(zhuǎn)移率與腫瘤部位、病理分化程度、病變X線長(zhǎng)度、pT分期以及淋巴結(jié)轉(zhuǎn)移數(shù)有關(guān)(P＜0.05)，但多因素Logistic回歸分析顯示，頸部淋巴結(jié)轉(zhuǎn)移率只與腫瘤部位、pT分期及淋巴結(jié)轉(zhuǎn)移數(shù)有關(guān)(P＜0.05)。本研究結(jié)果表明，頸部淋巴結(jié)轉(zhuǎn)移率隨腫瘤位置升高和總體淋巴結(jié)轉(zhuǎn)移數(shù)的增加而增高，建議對(duì)于胸上段食管癌和淋巴結(jié)轉(zhuǎn)移數(shù)較多者，應(yīng)常規(guī)給予頸部淋巴結(jié)轉(zhuǎn)移部位的治療。

近年來(lái)開(kāi)展的食管癌調(diào)強(qiáng)適形放療，可以提高生存率并減少放療并發(fā)癥［14］，但如何確定頸部淋巴結(jié)引流區(qū)亞臨床病灶是放療難點(diǎn)。本研究發(fā)現(xiàn)頸部淋巴結(jié)轉(zhuǎn)移有2個(gè)特點(diǎn)：①頸頸段食管旁淋巴結(jié)是最多見(jiàn)的轉(zhuǎn)移部位，其次是鎖骨上淋巴結(jié)，頸深淋巴結(jié)及咽后淋巴結(jié)少見(jiàn)，轉(zhuǎn)移與病變部位有關(guān)，部位越下轉(zhuǎn)移率越低；②各段食管癌右頸部淋巴結(jié)轉(zhuǎn)移明顯多于左頸部，與Akiyama等［2］報(bào)道相似。建議對(duì)胸上段食管癌在勾畫放療靶區(qū)時(shí)應(yīng)包括左右頸段食管旁及鎖骨上淋巴結(jié)引流區(qū)，對(duì)胸中段及下段食管癌應(yīng)酌情處理。

與傳統(tǒng)胸腹兩野清掃術(shù)相比，胸段食管癌頸胸腹三野淋巴結(jié)清掃術(shù)能提高生存率和降低術(shù)后局部復(fù)發(fā)率，但常規(guī)三野淋巴結(jié)清掃因有較高的手術(shù)并發(fā)癥而限制其廣泛應(yīng)用［2-3］。根據(jù)本研究結(jié)果和文獻(xiàn)報(bào)道建議對(duì)以下患者常規(guī)行頸部淋巴結(jié)清掃術(shù)：①胸上段食管癌［15］；②頸部彩超顯示頸部淋巴結(jié)短徑≥0.5 cm［16］；③喉返神經(jīng)旁淋巴結(jié)轉(zhuǎn)移者［11-13］。

綜上所述，胸段食管鱗癌頸部淋巴結(jié)轉(zhuǎn)移率較高，腫瘤部位、pT分期及淋巴結(jié)轉(zhuǎn)移數(shù)是影響頸部淋巴結(jié)轉(zhuǎn)移獨(dú)立因素；頸段食管旁淋巴結(jié)轉(zhuǎn)移最多見(jiàn)，其次是鎖骨上淋巴結(jié)轉(zhuǎn)移，頸深淋巴結(jié)及咽后淋巴結(jié)轉(zhuǎn)移少見(jiàn)；各段食管癌右頸淋巴結(jié)轉(zhuǎn)移明顯多于左頸轉(zhuǎn)移。

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Clinical analysis of the characteristics of cervical lymph node metastasis in thoracic esophageal squamous cell carcinoma

CHEN Jun-qiang1, ZHENG Xiong-wei2, ZHU Kun-shou3, LI Jian-cheng1, LIN Yu1, PAN Cai-zhu1, PAN Jian-ji1(1. Department of Radiation Oncology, Fujian Provincial Tumor Hospital, Teaching Hospital of Fujian Medical University, Fuzhou Fujian 350014, China; 2. Department of Pathology, Fujian Provincial Tumor Hospital, Teaching Hospital of Fujian Medical University, Fuzhou Fujian 350014, China; 3. Department of Thoracic Surgery, Fujian Provincial Tumor Hospital, Teaching Hospital of Fujian Medical University, Fuzhou Fujian 350014, China)

CHEN Jun-qiang E-mail: junqiangc@163.com

Background and purpose: Lymph node (LN) metastasis of esophageal cancer of neck rate higher, but there is little bulk reports. This article aimed to analyze the characteristics of cervical lymph node metastasis (CLN) in thoracic esophageal squamous cell carcinoma (TE-SCC) and the clinical role. Methods: A total number of 1 131 TE-SCC patients underwent radical esophagectomy plus three-field lymph node dissection at Fujian Provincial Tumor Hospital between Jan. 1993 to Dec. 2003, during which, 367 patients had pathological metastasis of CLN. Results: The metastatic rate of CLN was 33.2% for the entire group, 43.7%, 33.0% and 16.0% for the upper, middle and lower TE-SCC respectively. Single factor analysis showed that the metastatic rate of CLN was relevant with the tumor site, pathological differentiated degree, lesion length showed in X-ray, pT stage and the number of CLN (P＜0.05). But multivariate regression analysis showed that the metastatic rate of CLN was just relevant with the tumor site, pT stage and the number of CLN (P＜0.05). Metastasis of cervical paraesophageal lymph nodes was the most common, andsupraclavicular lymph node metastasis was next, and metastasis of cervical profound lymph nodes and retropharyngeal lymph nodes were rare. The ratio of the number of CLN occupied the sum of the segmental CLN were 57.7%, 32.0% and 10.0% for the upper, middle and lower TE-SCC respectively (P＜0.05). Right CLN of each segmental TE-SCC was more than left CLN. Conclusion: Independent factors on CLN in TE-SCC are the tumor site, pT stage and the number of CLN. Metastasis of cervical paraesophageal lymph nodes is the most common, and supraclavicular lymph node metastasis is next, and metastasis of cervical profound lymph nodes and retropharyngeal lymph nodes are rare.

Esophageal neoplasm; Cervical lymph node metastasis; Number of lymph node metastasis; Rate of lymph node metastasis

10.3969/j.issn.1007-3969.2013.11.012

R735.1

：A

：1007-3639(2013)11-0921-05

2013-05-02

2013-10-12）

福建省科技廳重點(diǎn)項(xiàng)目(2011Y0014)。

陳俊強(qiáng) E-mail:junqiangc@163.com