冯令军
[摘要] 目的 研究前哨淋巴结(sentinel lymph node, SLN)活检术(SLN biopsy, SLNB)对单侧多发乳腺癌(multiple synchronous tumor, MST)患者腋窝淋巴结状态判断的可行性。 方法 在23例确诊单侧多发乳腺癌患者术中行SLNB,所有患者均行乳腺癌改良根治术,如患者拒绝或者两病灶位于乳房同一象限,改行保乳加腋窝淋巴结清扫术(axillary lymphnode dissection, ALND)。术中不送检SLN,ALND后由手术医师分离出SLN送检。术后对全部淋巴结行连续切片病理检查。 结果 23例患者有21例完成前哨淋巴结活检术,成功率91.3%。SLN预测腋窝淋巴结状态的假阴性率、敏感度、准确率分别为15.4%,84.6%,90.5%。 结论 SLNB假阴性率高,不推荐在单侧多发乳腺癌患者中实行前哨淋巴结活检。
[关键词] 单侧;多发;乳腺癌;前哨淋巴结;腋窝淋巴结清扫
[中图分类号] R737.9 [文献标识码] B [文章编号] 1673-9701(2014)29-0152-03
A feasibility study of sentinel lymph node biopsy in preoperatively diagnosed multiple unilateral synchronous breast cancers
FENG Lingjun
Department of Thyroid Breast Surgery, Affiliated Hospital of Weifang Medical College, Weifang 261031, China
[Abstract] Objective To evaluate the feasibility of SLNB for predicting the status of axillary lymph node and determining the extent of axillary dissection in preoperatively diagnosed multiple unilateral synchronous breast cancers. Methods A total of 23 MST patients of clinical negative axillae diagnosed by core needle biopsy were studied. SLN was localized by injecting methylene blue. No intraoperative pathological examination. All patients with MST were eligible for initial breast surgery(radical modified mastectomy or conservative surgery+ALND). To choose radical modified mastectomy unless MST was limited to two foci in the same quadrant or patients opposition for total mastectomy). Sentinel lymph nodes (SLNs) were submitted to pathological doctor after ALND. All lymph nodes were valuated pathologically after operation. Results Of 23 patients, 21 cases were assessable. The SLNB-identified rate was 91.3%. The false-negative rate (FNR) was 15.4%, the accuracy rate was 90.5%, and the sensitivity was 84.6%. Conclusion With a high FNR,we do not recommend SLNB as a routine procedure for MST.
[Key words] Multifocal; Unilateral; Breast cancer; Sentinel node; Axillary lymphnode dissection
前哨淋巴结活检术(sentinel lymph node biopsy, SLNB)始于1994年,由Krag 及Giuliano最先报道[1,2],已被证实可替代腋窝淋巴清扫术(axillary lymphnode dissection,ALND),具有高精确性、低假阴性、低死亡率、低腋窝复发率等优点[3,4]。目前SLNB的适应证是早期浸润性肿瘤、且腋淋巴结临床评估为阴性的乳腺癌患者,禁忌证是炎性乳癌患者、临床腋窝淋巴结评估为N2期的患者。然而,关于SLNB的研究多局限于单发乳腺癌患者,多发乳腺癌(multiple synchronous tumor,MST )患者往往被排除于研究之外,因此对多发乳腺癌患者是否能够应用SLNB替代ALND意义不明确,本文即以此为契点进行研究,评估术前证实MST患者行SLNB的准确性及可行性。
1 资料与方法
1.1 临床资料
入选患者均为可手术的多发乳腺癌患者,所谓多发指术前经临床和/或影像学证实同一象限或者不同象限出现两个或者更多的肿块。术前所有患者均行乳房钼靶照相术及超声检查,必要时行磁共振检查。细针穿刺活检证实MST诊断。所有患者均采取乳腺癌改良根治术,除非患者拒绝或者两病灶位于乳房同一象限,改行保乳手术加腋窝淋巴结清扫术。非浸润癌、炎性乳癌、临床腋窝淋巴结(N1)、既往曾乳腺手术或曾接受肿瘤治疗者、手术后经病理学证实MST、妊娠者不在本研究之列。endprint
本研究共纳入2008年8月~2013年9月我院及合作医院收治的23例符合入选标准的患者,平均年龄(54.3±11.9)岁,中位年龄54.8岁。其中依据MRI明确诊断患者16例,依据其他检查措施明确诊断患者7例;明确诊断后行乳腺癌改良根治术患者20例,余3例行保乳+腋窝淋巴结清扫术;术前超声测量肿瘤直径< 20 mm 患者共计17例,≥ 20 mm者6例;术后经病理证实肿瘤数量为2个者15例,3个者7例,另有1例患者肿瘤数量证实为4个;术后证实最大肿瘤大小< 20 mm 患者15例,≥20 mm者8例;总肿瘤大小< 20 mm者 5例,≥20 mm者18例;16例患者术后病理类型显示为导管癌,6例患者为小叶癌,1例患者为髓样癌。
1.2 淋巴结示踪技术
1.2.1 淋巴示踪材料 选用江苏济川制药厂生产的1%亚甲蓝注射液(美蓝)。批准文号:苏卫药准字(1989)第216102号。规格:2 mL:20 mg。
1.2.2 SLN的定位活检方法 患者平卧,患侧上肢外展90°,常规消毒铺巾,采用乳晕下注射亚甲蓝 2 mL示踪,注射后对局部稍加压按摩,静待10~15 min后,于手术外弧线切开近腋处,锐性游离皮瓣,在胸大肌外缘与胸壁交界处,钝性分离腋深部软组织,寻找蓝染的淋巴管,钝性分离并解剖出蓝染的淋巴结(中多名手术医生共同确定,术中术者以肉眼辨别出蓝染淋巴结,认为前哨淋巴结寻找成功,术中未找到蓝染淋巴结,无论术后在腋窝组织的标本中是否找到蓝染淋巴结,均认为寻找失败;术中找到蓝染淋巴管,但未找到蓝染淋巴结者也认为寻找失败)。SLNB后,所有患者均行Ⅰ~Ⅱ级淋巴结清扫术。术后对所有腋窝淋巴结(包括SLN)做连续石蜡切片病理检查。
1.2.3病理学分析 术中不送检病理。ALND后由手术医师分离出SLN送检。所有清扫淋巴结均送检,连续切片,石蜡包埋。其中SLN连续切片6张,切片间隔150 μm。检测时除HE染色外还行免疫组化染色。非SLN行HE染色,未行免疫组化染色。病理报告包括腋窝前哨淋巴结数量,总淋巴结数量及转移灶(>2 mm)、微转移灶(0.2~2 mm)、孤立肿瘤细胞数量(<0.2 mm),使用AJC肿瘤分期标准。术中切除的乳房浸泡固定于10%福尔马林溶液中,连续切片,间隔1.0 cm。触诊或影像学高度可疑多病灶患者,依据肿瘤数量、肿瘤间有无正常组织进一步确诊。
1.3 统计学方法
参照美国Louisville大学标准[5]计算,检出率= SLN检出例数/实施SLN检测所有例数×100%,准确率=(SLN真阳性+真阴性例数)/SLN活检总例数×100%,敏感度=SLN真阳性/(真阳性+假阴性)×100%,假阴性率=SLN假阴性/(真阳性+假阴性)×100%,阴性预测值=真阴性/(真阴性+假阴性)。分析的单位为病例数而非切除的淋巴结数。准确率、敏感度、假阴性率、阴性预测值及其95%可信区间(95% confidence intervals,95%CIs)均按二项分布原理计算。
2 结果
2.1 SLN检出率
23例患者中21例完成SLNB,成功率 91.3%,2例未完成者均行腋窝淋巴结清扫术,其中1例患者术中及术后病理检出多于3枚转移淋巴结。1例患者未检出转移淋巴结。前哨淋巴结平均检出数为2.5枚(1~7,±1.3),腋窝淋巴结清扫术证实平均淋巴结转移数为11.7枚(1~35,±6.2)。
2.2 SLNB病理学结果及意义
SLNB及ALND结果见图1。
图1 多发乳腺癌患者SLNB结果示意图
由图1可知,无论腋窝淋巴结清扫还是前哨淋巴结活检至少1枚淋巴结阳性的患者数占总活检人数的60.9 %(14/23),其中11例经前哨淋巴结活检证实。前哨淋巴结阳性的患者中,5例腋窝淋巴结清扫术证实多枚淋巴结转移(5/11,45.5%)。前哨淋巴结活检未见异常的10例患者中,2例腋窝淋巴结清扫证实至少1枚淋巴结受侵犯。假阴性率为2/13,15.4 %(95%CIs 为2%~45%),敏感率 11/13,84.6%(95%CIs为55%~98%),阴性预测值为 8/10,80%(95%CIs为44%- 97%),准确率为19/21,90.5%(95%CIs为70%~99%)。SLN阳性的11例患者中,7例患者(63.6%)转移灶>2 mm,3例患者发现微转移灶(27.3%),剩余1例患者孤立肿瘤细胞阳性(9.1%)。
3 讨论
乳腺癌前哨淋巴结活检(SLNB)是乳腺外科领域的一个里程碑式的进展。乳腺癌的前哨淋巴结是指位于乳腺癌淋巴引流途径上距引流区域最近的淋巴结,因而当乳腺癌发生淋巴转移时,前哨淋巴结将是第一个包含转移灶的淋巴结,然后再引流到下一站淋巴结。其包括2个含义:一是前哨淋巴结为第一个受癌细胞侵袭的淋巴结;二是前哨淋巴结的病理状态可准确预测该区域其他淋巴结的病理状态,尤其是前哨淋巴结阴性时可排除其淋巴引流区域其他淋巴结的癌转移。但是前哨淋巴结阴性时,该肿瘤淋巴引流区域的其他淋巴结可有癌转移,而这种现象是罕见的,在早期肿瘤其发生率更低。
现代研究普遍认为单病灶乳腺浸润性癌患者行SLNB可替代常规ALND[3,6-8],然而对多发癌肿患者,SLNB的应用研究甚少,绝大部分研究入选标准即除外多发患者。既往研究认为不同象限的肿瘤引流至不同淋巴结[9]。最近几年的研究发现,不同象限肿瘤可能引流至同一淋巴结[10,11]。目前对多发乳腺癌患者,SLNB研究意义尚不明确,未列入适应证或者禁忌证中。对于多发癌肿患者能否行SLNB替代ALND,各项研究意见不一,是乳癌治疗的研究热点之一。本研究即着眼于此,试图进一步明确SLNB对多发乳腺癌患者有无临床意义,能否替代ALND,以减少患者痛苦,提高生存质量。endprint
本研究SLN检出率91.3%,这与国外研究报道的哨兵淋巴结鉴别成功率66%~98%相符[12],分析本研究不能完全检出前哨淋巴结的原因可能在于早期推注美蓝力量掌握不够,造成疏松的后间隙大片蓝染,致使前哨淋巴结不能检出,这也反映了掌握此项技术的正常学习曲线。同时50岁以上妇女淋巴管功能退化,吸收转运功能差,淋巴结内的淋巴组织被脂肪组织所替代,淋巴结内网状内皮细胞的吞噬功能和机械屏障减弱,减少其对染料的滞留,从而影响前哨淋巴结的检出率[13,14]。
SLN活检技术的可行性是建立在SLN预测腋窝淋巴结转移情况的敏感性大于85%,假阴性率低于15%的基础上的[15]。我们的研究发现,多发乳腺癌患者淋巴结阳性率为60.9%,这与其他多发乳腺癌患者淋巴结阳性率文献报道相符[16],但多发乳腺癌患者行SLNB,其FNR达15.4%。与单发乳腺癌患者SLN预测淋巴结转移相比,本研究预测淋巴结转移情况的敏感性、准确性降低,而假阴性率增高,阴性预测的准确性下降,而SLN假阴性结果会导致错误的治疗方案,有可能产生严重的不良后果,因此,不推荐在多发乳腺癌患者中实行SLNB。本研究进一步明确了SLNB的临床适应证不应包括多发乳腺癌患者。
综上,尽管多发性乳腺癌患者行SLNB微创,但其假阴性率较高,易造成漏诊、误诊,因此不推荐在多发乳腺癌患者中实行SLNB替代ALND。
[参考文献]
[1] Krag DN,Weaver DL,Alex JC,et al. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe[J]. Surg Oncol,1993,2(6): 335-339.
[2] Giuliano AE,Kirgan DM,Guenther JM,et al. Lymphatic mapping and sentinel lymphadenectomy for breast cancer[J].Ann Surg,1994,220(3):391-398.
[3] Gary H L,Sarah T,Stephen BE,et al. Sentinel lymph node biopsy for patients with early-stage breast cancer: American society of clinical oncology clinical practice guideline update[J]. J Clin Oncol,2014,32(13):1365-1383.
[4] Electra DP,Julie AD,Jill MO,et al. Cancer-related lymphedema risk factors,diagnosis,treatment,and impact:A review[J]. J Clin Oncol,2012,30(30):3726-3733.
[5] 尉承泽. 乳腺癌哨兵淋巴结检测[J]. 国外医学:肿瘤学分册,2003,30(2):104-106.
[6] Giard S,Chauvet MP,Penel N,et al. Feasibility of sentinel lymph node biopsy in multiple unilateral synchronous breast cancer: results of a French prospective multi-institutional study(IGASSU 0502)[J]. Ann Oncol,2010,21(8):1630-1635.
[7] White V,Harvey JR,Griffith CDM,et al. Sentinel lymph node biopsy in early breast cancer surgery-Working with the risks of vital blue dye to reap the benefits[J]. Eur J Surg Onc ,2011,37(2):101-108.
[8] Belinda Y,Nicholas CT,Alison J. An update on the medical management of breast cancer[J]. BMJ,2014,348:3608.
[9] Elif H,David G,Isabelle BR,et al. The sentinel node procedure in breast ccancer: Nuclear medicine as the starting point[J]. J Nucl Med,2011,52(3):405-414.
[10] Bernsdorf M,Berthelsen AK,Wielenga VT,et al. Preoperative PET/CT in early-stage breast cancer[J]. Ann Oncol,2012,23(9):2277-2282.
[11] Moody LC,Wen X,McKnight T,et al Indications for sentinel lymph node biopsy in multifocal and multicentric breast cancer[J]. Surg,2012,152(3):389-396.
[12] Christoph H,Holger E,Leila K,et al. An experimental study to evaluate the fluobeam 800 imaging system for fluorescence-guided lymphatic imaging and sentinel node biopsy[J]. Surg Innov, 2013,20(5): 516-523.
[13] Kang SS,Han BK,Ko EY,et al. Methylene blue dye-related changes in the breast after sentinel lymph node localization[J]. J Ultra Med,2011,30(12):1711-1721.
[14] Hye SA,Sun MK,Mijung J,et al. Comparison of sonography with sonographically guided fine-needle aspiration biopsy and core-needle biopsy for initial axillary stsaging of breast cancer[J]. J Ultra Med,2013,32(12):2177-2184.
[15] 张保宁,白月奎,陈国际,等. 乳腺癌前哨淋巴结活检的临床意义[J]. 中华肿瘤杂志,2000,22(5):395-397.
[16] Moghimi1 M,Ghoddosi1 I,Rahimabadi1 AE,et al. Accuracy of sentinel node biopsy in breast cancer patients with a high prevalence of axillary metastases[J]. Scan J of Surg,2009,98(1):30-33.
(收稿日期:2014-06-09)endprint
本研究SLN检出率91.3%,这与国外研究报道的哨兵淋巴结鉴别成功率66%~98%相符[12],分析本研究不能完全检出前哨淋巴结的原因可能在于早期推注美蓝力量掌握不够,造成疏松的后间隙大片蓝染,致使前哨淋巴结不能检出,这也反映了掌握此项技术的正常学习曲线。同时50岁以上妇女淋巴管功能退化,吸收转运功能差,淋巴结内的淋巴组织被脂肪组织所替代,淋巴结内网状内皮细胞的吞噬功能和机械屏障减弱,减少其对染料的滞留,从而影响前哨淋巴结的检出率[13,14]。
SLN活检技术的可行性是建立在SLN预测腋窝淋巴结转移情况的敏感性大于85%,假阴性率低于15%的基础上的[15]。我们的研究发现,多发乳腺癌患者淋巴结阳性率为60.9%,这与其他多发乳腺癌患者淋巴结阳性率文献报道相符[16],但多发乳腺癌患者行SLNB,其FNR达15.4%。与单发乳腺癌患者SLN预测淋巴结转移相比,本研究预测淋巴结转移情况的敏感性、准确性降低,而假阴性率增高,阴性预测的准确性下降,而SLN假阴性结果会导致错误的治疗方案,有可能产生严重的不良后果,因此,不推荐在多发乳腺癌患者中实行SLNB。本研究进一步明确了SLNB的临床适应证不应包括多发乳腺癌患者。
综上,尽管多发性乳腺癌患者行SLNB微创,但其假阴性率较高,易造成漏诊、误诊,因此不推荐在多发乳腺癌患者中实行SLNB替代ALND。
[参考文献]
[1] Krag DN,Weaver DL,Alex JC,et al. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe[J]. Surg Oncol,1993,2(6): 335-339.
[2] Giuliano AE,Kirgan DM,Guenther JM,et al. Lymphatic mapping and sentinel lymphadenectomy for breast cancer[J].Ann Surg,1994,220(3):391-398.
[3] Gary H L,Sarah T,Stephen BE,et al. Sentinel lymph node biopsy for patients with early-stage breast cancer: American society of clinical oncology clinical practice guideline update[J]. J Clin Oncol,2014,32(13):1365-1383.
[4] Electra DP,Julie AD,Jill MO,et al. Cancer-related lymphedema risk factors,diagnosis,treatment,and impact:A review[J]. J Clin Oncol,2012,30(30):3726-3733.
[5] 尉承泽. 乳腺癌哨兵淋巴结检测[J]. 国外医学:肿瘤学分册,2003,30(2):104-106.
[6] Giard S,Chauvet MP,Penel N,et al. Feasibility of sentinel lymph node biopsy in multiple unilateral synchronous breast cancer: results of a French prospective multi-institutional study(IGASSU 0502)[J]. Ann Oncol,2010,21(8):1630-1635.
[7] White V,Harvey JR,Griffith CDM,et al. Sentinel lymph node biopsy in early breast cancer surgery-Working with the risks of vital blue dye to reap the benefits[J]. Eur J Surg Onc ,2011,37(2):101-108.
[8] Belinda Y,Nicholas CT,Alison J. An update on the medical management of breast cancer[J]. BMJ,2014,348:3608.
[9] Elif H,David G,Isabelle BR,et al. The sentinel node procedure in breast ccancer: Nuclear medicine as the starting point[J]. J Nucl Med,2011,52(3):405-414.
[10] Bernsdorf M,Berthelsen AK,Wielenga VT,et al. Preoperative PET/CT in early-stage breast cancer[J]. Ann Oncol,2012,23(9):2277-2282.
[11] Moody LC,Wen X,McKnight T,et al Indications for sentinel lymph node biopsy in multifocal and multicentric breast cancer[J]. Surg,2012,152(3):389-396.
[12] Christoph H,Holger E,Leila K,et al. An experimental study to evaluate the fluobeam 800 imaging system for fluorescence-guided lymphatic imaging and sentinel node biopsy[J]. Surg Innov, 2013,20(5): 516-523.
[13] Kang SS,Han BK,Ko EY,et al. Methylene blue dye-related changes in the breast after sentinel lymph node localization[J]. J Ultra Med,2011,30(12):1711-1721.
[14] Hye SA,Sun MK,Mijung J,et al. Comparison of sonography with sonographically guided fine-needle aspiration biopsy and core-needle biopsy for initial axillary stsaging of breast cancer[J]. J Ultra Med,2013,32(12):2177-2184.
[15] 张保宁,白月奎,陈国际,等. 乳腺癌前哨淋巴结活检的临床意义[J]. 中华肿瘤杂志,2000,22(5):395-397.
[16] Moghimi1 M,Ghoddosi1 I,Rahimabadi1 AE,et al. Accuracy of sentinel node biopsy in breast cancer patients with a high prevalence of axillary metastases[J]. Scan J of Surg,2009,98(1):30-33.
(收稿日期:2014-06-09)endprint
本研究SLN检出率91.3%,这与国外研究报道的哨兵淋巴结鉴别成功率66%~98%相符[12],分析本研究不能完全检出前哨淋巴结的原因可能在于早期推注美蓝力量掌握不够,造成疏松的后间隙大片蓝染,致使前哨淋巴结不能检出,这也反映了掌握此项技术的正常学习曲线。同时50岁以上妇女淋巴管功能退化,吸收转运功能差,淋巴结内的淋巴组织被脂肪组织所替代,淋巴结内网状内皮细胞的吞噬功能和机械屏障减弱,减少其对染料的滞留,从而影响前哨淋巴结的检出率[13,14]。
SLN活检技术的可行性是建立在SLN预测腋窝淋巴结转移情况的敏感性大于85%,假阴性率低于15%的基础上的[15]。我们的研究发现,多发乳腺癌患者淋巴结阳性率为60.9%,这与其他多发乳腺癌患者淋巴结阳性率文献报道相符[16],但多发乳腺癌患者行SLNB,其FNR达15.4%。与单发乳腺癌患者SLN预测淋巴结转移相比,本研究预测淋巴结转移情况的敏感性、准确性降低,而假阴性率增高,阴性预测的准确性下降,而SLN假阴性结果会导致错误的治疗方案,有可能产生严重的不良后果,因此,不推荐在多发乳腺癌患者中实行SLNB。本研究进一步明确了SLNB的临床适应证不应包括多发乳腺癌患者。
综上,尽管多发性乳腺癌患者行SLNB微创,但其假阴性率较高,易造成漏诊、误诊,因此不推荐在多发乳腺癌患者中实行SLNB替代ALND。
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(收稿日期:2014-06-09)endprint