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中华乳腺病杂志(电子版)

中华乳腺病杂志(电子版) ›› 2020, Vol. 14 ›› Issue (01) : 23 -31. doi: 10.3877/cma.j.issn.1674-0807.2020.01.008

所属专题： 文献；

论著

脉管癌栓中间质细胞/癌细胞、巨噬细胞/癌细胞比值与pT1～4N1～3M0期乳腺癌患者临床病理特征及预后的关系
范丽娟1, 王嘉2, 高雪3, 毛晓韵1, 王旭1, 郑昂1, 马楠4, 金锋1,†()   
  1. 1. 110001　沈阳，中国医科大学附属第一医院乳腺外科
    2. 116000　大连医科大学附属第二医院乳腺外科
    3. 116000　大连医科大学附属第一医院病理科
    4. 110001　沈阳，北部战区总医院肿瘤科
  • 收稿日期:2019-03-12 出版日期:2020-02-01
  • 通信作者: 金锋
  • 基金资助:
    国家自然科学基金资助项目(81773163、81602309)

Relationship between the ratio of mesenchymal cells or macrophages to cancer cells in lymphovascular invasion and clinicopathologic features and prognosis of pT1-4N1-3M0 breast cancer patients

Lijuan Fan1, Jia Wang2, Xue Gao3, Xiaoyun Mao1, Xu Wang1, Ang Zheng1, Nan Ma4, Feng Jin1,†()   

  1. 1. Department of Breast Surgery, First Affiliated Hospital of China Medical University, Shenyang 110001, China
    2. Department of Breast Surgery, Second Hospital of Dalian Medical University, Dalian 116000, China
    3. Department of Pathology, First Affiliated Hospital of Dalian Medical University, Dalian 116000, China
    4. Department of Oncology, Northern Theater General Hospital of PLA, Shenyang 110001, China
  • Received:2019-03-12 Published:2020-02-01
  • Corresponding author: Feng Jin
  • About author:
    Corresponding author: Jin Feng, Email:
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引用本文：

范丽娟, 王嘉, 高雪, 毛晓韵, 王旭, 郑昂, 马楠, 金锋. 脉管癌栓中间质细胞/癌细胞、巨噬细胞/癌细胞比值与pT1～4N1～3M0期乳腺癌患者临床病理特征及预后的关系[J]. 中华乳腺病杂志(电子版), 2020, 14(01): 23-31.

Lijuan Fan, Jia Wang, Xue Gao, Xiaoyun Mao, Xu Wang, Ang Zheng, Nan Ma, Feng Jin. Relationship between the ratio of mesenchymal cells or macrophages to cancer cells in lymphovascular invasion and clinicopathologic features and prognosis of pT1-4N1-3M0 breast cancer patients[J]. Chinese Journal of Breast Disease(Electronic Edition), 2020, 14(01): 23-31.

目的

探讨脉管癌栓中间质细胞/癌细胞比值、巨噬细胞/癌细胞比值与pT1～4N1～3M0期乳腺癌患者临床病理特征及预后的关系。

方法

采用回顾性研究方法，选取2013年1月至2015年12月在中国医科大学附属第一医院及大连医科大学附属第一、二医院经系统治疗并有完整随访资料的167例pT1～4N1～3M0期腋窝淋巴结阳性乳腺癌患者作为研究对象，中位随访55.2个月(16.8～69.6个月)。采用免疫组织化学染色方法分别检测脉管癌栓中间质细胞和巨噬细胞的数目，计算间质细胞/癌细胞比值及巨噬细胞/癌细胞比值，采用Ward法分别对间质细胞/癌细胞比值和巨噬细胞/癌细胞比值进行聚类，得到低比值和高比值两类。分别采用Kruskal-Wallis H检验、χ2检验分析该比值与患者临床病理特征的关系，并用log-rank检验分析该比值与患者预后的关系。

结果

167例患者间质细胞/癌细胞、巨噬细胞/癌细胞比值的M(P25～P75)分别为0.025(0.015～0.063)和0.023(0.015～0.036)。间质细胞/癌细胞比值与患者的组织学分级、肿瘤大小、腋窝淋巴结转移状态、临床分期及脉管浸润有关(χ2＝10.210、6.210、64.315、56.901、19.771，P＝0.001、0.045及P均<0.001)，但与ER、PR、HER-2、Ki67表达及神经侵犯无关(χ2＝3.148、2.260、3.187、0.145、1.384，P＝0.076、0.133、0.074、0.704、0.240)；巨噬细胞/癌细胞比值与患者的肿瘤大小、ER表达、神经侵犯、组织学分级、腋窝淋巴结转移状态、临床分期、脉管浸润和HER-2表达有关(χ2＝7.487、6.680、8.439、13.002、25.856、31.394、19.771、27.921，P＝0.024、0.010、0.004及P均<0.001)，但与PR、Ki67表达无关(χ2＝3.616、1.183，P＝0.057、0.277)。聚类后间质细胞/癌细胞比值与腋窝淋巴结转移状态及临床分期均有关系(χ2＝47.300，P<0.001；χ2＝14.260，P＝0.001)，而巨噬细胞/癌细胞比值仅与ER表达有关(χ2＝5.136，P＝0.023)。间质细胞/癌细胞、巨噬细胞/癌细胞比值均与乳腺癌患者DFS率相关，比值越高者DFS率越低(预后越差)(χ2＝24.124、18.746，P均<0.001)。

结论

脉管癌栓中间质细胞/癌细胞比值和巨噬细胞/癌细胞比值高的患者预后不良，此比值可作为评价pT1－4N1－3M0期乳腺癌患者复发风险的参考指标。

关键词: 间质细胞, 巨噬细胞, 乳腺肿瘤, 存活率, 预后, 脉管癌栓, 肿瘤微环境
Objective

To investigate the relationship between the ratio of mesenchymal cells to cancer cells or macrophages to cancer cells in lymphovascular invasion (LVI) and clinicopathologic features and prognosis of pT1-4N1-3M0 breast cancer patients.

Methods

A total of 167 pT1-4N1-3M0 breast cancer patients who received systemic treatment and had complete follow-up data in the First Affiliated Hospital of China Medical University, the First and Second Affiliated Hospitals of Dalian Medical University from January 2013 to December 2015 were enrolled in this retrospective study, with a median follow-up period of 55.2 months (16.8-69.6 months). Immunohistochemistry was used to identify the number of mesenchymal cells or macrophages in LVI. The ratio of mesenchymal cells to cancer cells and the ratio of macrophages to cancer cells in LVI were calculated. The Ward clustering method was used to divide the patients into two groups: high-ratio group and low-ratio group. Kruskal-Wallis H test and χ2 test were used to analyze the relationship between the ratios and clinicopathologic features of breast cancer patients; the log-rank test was used to analyze the relationship between the ratios and the patient prognosis.

Results

The ratios [M(P25-P75)] of mesenchymal cells to cancer cells and macrophages to cancer cells in 167 patients were 0.025 (0.015-0.063) and 0.023 (0.015-0.036), respectively. The ratio of mesenchymal cells to cancer cells was correlated with histological grade, tumor size, lymph node metastasis, clinical stage and LVI (χ2=10.210, 6.210, 64.315, 56.901, 19.771; P=0.001, 0.045, and all P<0.001), but not correlated with ER, PR, HER-2, Ki67 expression and nerve invasion (χ2=3.148, 2.260, 3.187, 0.145, 1.384; P=0.076, 0.133, 0.074, 0.704, 0.240). The ratio of macrophages to cancer cells was correlated with tumor size, ER expression, nerve invasion, histological grade, lymph node metastasis, clinical stage, LVI and HER-2 expression(χ2=7.487, 6.680, 8.439, 13.002, 25.856, 31.394, 19.771, 27.921; P=0.024, 0.010, 0.004, all P<0.001), but not correlated with Ki67 and PR expression (χ2=3.616, 1.183; P=0.057, 0.277). After clustering, the ratio of mesenchymal cells to cancer cells was related to lymph node metastasis and clinical stage (χ2=47.3, P<0.001; χ2=14.260, P=0.001); the ratio of macrophages to cancer cells was related to ER expression (χ2=5.136, P=0.023). The patients with a higher ratio of mesenchymal cells or macrophages to cancer cells in LVI had a lower DFS (worse prognosis) (χ2=24.124, 18.746, both P<0.001).

Conclusion

High ratio of mesenchymal cells or macrophages to cancer cells in LVI suggests poor prognosis, so the ratio could serve as an indicator for recurrence risk of pT1-4N1-3M0 breast cancer patients.

Key words: Mesenchymal cells, Macrophages, Breast neoplasms, Survival rate, Prognosis, Lymphovascular invasion, Tumor microenvironment
图1 乳腺癌患者脉管癌栓中间质细胞vimentin的免疫组织化学染色(SP ×400)
图2 乳腺癌患者脉管癌栓中巨噬细胞的白细胞分化抗原68免疫组织化学染色(SP ×400)
表1 乳腺癌患者临床病理特征与间质细胞/癌细胞、巨噬细胞/癌细胞比值的关系[M(P25～P75)]
临床病理特征 例数 间质细胞/癌细胞比值 χ2值a P值 巨噬细胞/癌细胞比值 χ2值a P值
组织学分级 ? ? ? ? ? ? ?
? 2级 102 0.021(0.012～0.045) 10.210 0.001 0.020(0.013～0.031) 13.002 <0.001
? 3级 65 0.039(0.020～0.082) 0.030(0.019～0.042)
肿瘤大小 ? ? ? ? ? ? ?
? 1～10 mm 55 0.022(0.012～0.073) 6.210 0.045 0.019(0.012～0.035) 7.487 0.024
? 11～20 mm 95 0.021(0.015～0.058) 0.023(0.015～0.033)
? >20 mm 17 0.045(0.026～0.078) 0.031(0.025～0.052)
腋窝淋巴结转移 ? ? ? ? ? ? ?
? 1枚 46 0.015(0.012～0.025) 64.315 <0.001 0.015(0.010～0.023) 25.856 <0.001
? 2～3枚 57 0.018(0.013～0.025) 0.022(0.015～0.032)
? 4～5枚 35 0.044(0.023～0.058) 0.027(0.020～0.041)
? >5枚 29 0.110(0.074～0.140) 0.034(0.025～0.049)
临床分期 ? ? ? ? ? ? ?
? Ⅰ期 16 0.012(0.010～0.014) 56.901 <0.001 0.011(0.008～0.015) 31.394 <0.001
? Ⅱ期 86 0.018(0.013～0.028) 0.021(0.015～0.031)
? Ⅲ期 65 0.057(0.036～0.113) 0.031(0.022～0.044)
脉管浸润 ? ? ? ? ? ? ?
? 无 7 0(0) 19.771 <0.001 0(0) 19.771 <0.001
? 有 160 0.025(0.016～0.065) 0.024(0.016～0.039)
ER ? ? ? ? ? ? ?
? 阴性 48 0.037(0.018～0.080) 3.148 0.076 0.031(0.019～0.043) 6.68 0.010
? 阳性 119 0.021(0.014～0.057) 0.021(0.014～0.031)
PR ? ? ? ? ? ? ?
? 阴性 77 0.035(0.016～0.075) 2.260 0.133 0.024(0.017～0.042) 3.616 0.057
? 阳性 90 0.021(0.014～0.052) 0.021(0.014～0.031)
HER-2 ? ? ? ? ? ? ?
? 阴性 130 0.021(0.014～0.061) 3.187 0.074 0.021(0.014～0.029) 27.921 <0.001
? 阳性 37 0.039(0.018～0.078) 0.042(0.031～0.050)
Ki67 ? ? ? ? ? ? ?
? 阴性 69 0.023(0.014～0.057) 0.145 0.704 0.022(0.015～0.031) 1.183 0.277
? 阳性 98 0.026(0.015～0.075) 0.024(0.015～0.041)
神经侵犯 ? ? ? ? ? ? ?
? 无 137 0.026(0.015～0.069) 1.384 0.240 0.025(0.016～0.041) 8.439 0.004
? 有 30 0.020(0.015～0.047) 0.016(0.012～0.026)
表2 乳腺癌患者间质细胞/癌细胞、巨噬细胞/癌细胞比值聚类结果的统计学意义验证
聚类分析 例数 间质(巨噬)细胞/癌细胞比值[M(P25～P75)] χ2值a P值
间质细胞聚类 ? ? ? ?
? 低比值组 140 0.021(0.013～0.041) 67.571 <0.001
? 高比值组 27 0.142(0.116～0.172)
巨噬细胞聚类 ? ? ? ?
? 低比值组 151 0.021(0.014～0.031) 43.186 <0.001
? 高比值组 16 0.088(0.072～0.113)
表3 乳腺癌患者临床病理特征与聚类后间质细胞/癌细胞、巨噬细胞/癌细胞比值的关系[例(%)]
临床病理特征 例数 间质细胞/癌细胞 χ2值 P值 巨噬细胞/癌细胞 χ2值 P值
低比值 高比值 低比值 高比值
组织学分级 ? ? ? ? ? ? ? ? ?
? 2级 102 90(88.2) 12(11.8) 3.748 0.053 93(91.2) 9(8.8) 0.173 0.677
? 3级 65 50(76.9) 15(23.1) 58(89.2) 7(10.8)
肿瘤大小 ? ? ? ? ? ? ? ? ?
? 1～10 mm 55 47(85.5) 8(14.5) 0.797 0.671 51(92.7) 4(7.3) 4.304 0.116
? 11～20 mm 95 80(84.2) 15(15.8) 87(91.6) 8(8.4)
? >20 mm 17 13(13/17a) 4(4/17a) 13(13/17a) 4(4/17a)
腋窝淋巴结转移 ? ? ? ? ? ? ? ? ?
? 1枚 46 43(93.5) 3(6.5) 47.300 <0.001 43(93.5) 3(6.5) 5.993 0.112
? 2～3枚 57 54(94.7) 3(5.3) 54(94.7) 3(5.3)
? 4～5枚 35 31(88.6) 4(11.4) 31(88.6) 4(11.4)
? >5枚 29 12(41.4) 17(58.6) 23(79.3) 6(20.7)
临床分期 ? ? ? ? ? ? ? ? ?
? Ⅰ期 16 16(16/16a) 0(0) 14.260 0.001 16(16/16a) 0(0) 3.267 0.195
? Ⅱ期 86 78(90.7) 8(9.3) 79(91.9) 7(8.1)
? Ⅲ期 65 46(70.8) 19(29.2) 56(86.2) 9(13.8)
脉管浸润 ? ? ? ? ? ? ? ? ?
? 无 7 7(7/7a) 0(0) 0.439 0.508 7(7/7a) 0(0) ? 1.000b
? 有 160 133(83.1) 27(16.9) 144(90.0) 16(10.0)
ER ? ? ? ? ? ? ? ? ?
? 阴性 48 40(83.3) 8(16.7) 0.012 0.991 39(81.2) 9(18.8) 5.136 0.023
? 阳性 119 100(84.0) 19(16.0) 112(94.1) 7(5.9)
PR ? ? ? ? ? ? ? ? ?
? 阴性 77 64(83.1) 13(16.9) 0.054 0.816 67(87.0) 10(13.0) 1.914 0.167
? 阳性 90 76(84.4) 14(15.6) 84(93.3) 6(6.7)
HER-2 ? ? ? ? ? ? ? ? ?
? 阴性 130 109(83.8) 21(16.2) <0.001 0.993 120(92.3) 10(7.7) 1.532 0.216
? 阳性 37 31(83.8) 6(16.2) 31(83.8) 6(16.2)
Ki67 ? ? ? ? ? ? ? ? ?
? 阴性 69 59(85.5) 10(14.5) 0.243 0.622 64(92.8) 5(7.2) 0.740 0.390
? 阳性 98 81(82.7) 17(17.3) 87(88.8) 11(11.2)
神经侵犯 ? ? ? ? ? ? ? ? ?
? 无 137 113(82.5) 24(17.5) 0.547 0.460 121(88.3) 16(11.7) 2.644 0.104
? 有 30 27(90.0) 3(10.0) 30(100) 0(0)
图3 乳腺癌患者无瘤生存率与间质细胞/癌细胞比值的关系
图4 乳腺癌患者无瘤生存率与巨噬细胞/癌细胞比值的关系
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