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Article(id=1198196211661505132, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198196207379120715, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.0574.2023.0911, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1681833600000, receivedDateStr=2023-04-19, revisedDate=null, revisedDateStr=null, acceptedDate=1684339200000, acceptedDateStr=2023-05-18, onlineDate=1763601838268, onlineDateStr=2025-11-20, pubDate=1735315200000, pubDateStr=2024-12-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1763601838268, onlineIssueDateStr=2025-11-20, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1763601838268, creator=13701087609, updateTime=1763601838268, updator=13701087609, issue=Issue{id=1198196207379120715, tenantId=1146029695717560320, journalId=1189873630562394117, year='2024', volume='49', issue='12', pageStart='1343', pageEnd='1459', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1763601837248, creator=13701087609, updateTime=1763603898104, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1198204851306988030, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198196207379120715, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1198204851306988031, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198196207379120715, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=1386, endPage=1393, ext={EN=ArticleExt(id=1198196211963495030, articleId=1198196211661505132, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=The value of tumor associated neutrophils and neutrophil to lymphocyte ratio in evaluating the efficacy and prognosis of neoadjuvant chemotherapy for breast cancer, columnId=1190310109000602400, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Clinical Research, runingTitle=null, highlight=null, articleAbstract=

Objective To investigate the value of CD66b+ tumor-associated neutrophils (TANs) and neutrophil to lymphocyte ratio (NLR) in evaluating the efficacy and prognosis of neoadjuvant chemotherapy (NACT) for breast cancer. Methods One hundred and sixty-seven patients of invasive breast cancer treated with NACT in the Department of Breast Surgery, the First People Hospital of Lianyungang from January 2015 to June 2020 were collected, and 40 cases of normal breast tissues were collected. Immunohistochemistry was used to detect the expression of CD66b in breast cancer tissues before NACT and normal breast tissues. Peripheral venous blood was taken from patients within 1 week before the first cycle of NACT, count neutrophils and lymphocytes were counted and their ratio (NLR) was calculated. The correlation between TANs and NLR and clinicopathologic features was analyzed by χ2 test. The influencing factors of efficacy of NACT were analyzed by univariate χ2 test and multivariate logistic analysis. Kaplan-Meier survival analysis and multivariate Cox analysis were used to determine the prognostic factors. The correlation between TANs and NLR was determined by Spearman test. Results The expression of CD66b in breast cancer tissues was significantly higher than that in normal breast tissues (P<0.05), and it was diffusely distributed throughout the tumor (cancer nest and stroma were infiltrated). High infiltration of parenchymal TANs before NACT was correlated with high clinical stage, lymph node metastasis, and recurrence and metastasis (P<0.05). High NLR before NACT was closely related to high cT stage and recurrence and metastasis (P<0.05). NLR of peripheral blood (P=0.007), cT stage (P=0.041), estrogen receptor (ER) status (P=0.009), and human epidermal growth factor 2 (HER2) expression (P=0.020) were independent predictors for pathologic complete response (pCR). TANs (P=0.023), high clinical stage (P=0.040), and pCR (P=0.027) before NACT were independent risk factors for disease-free survival (DFS) of patients with invasive breast cancer. There was no correlation between NLR and TANs (r=0.14, P=0.071). Conclusions Low infiltration of parenchymal TANs before NACT predicts a better prognosis for patients with breast cancer. Higher NLR in peripheral blood is associated with chemotherapy resistance.

, correspAuthors=Shu-Qin Li, authorNote=null, correspAuthorsNote=
E-mail:
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目的 探讨CD66b+ 肿瘤相关中性粒细胞(TANs)和中性粒细胞与淋巴细胞比值(NLR)对乳腺癌新辅助化疗(NACT)疗效及预后的评估价值。方法 回顾性收集2015年1月－2020年6月在连云港市第一人民医院乳腺外科接受NACT治疗的167例浸润性乳腺癌患者的乳腺癌组织，同时收集正常乳腺组织40例作为对照。采用免疫组化染色检测NACT前乳腺癌组织和正常乳腺组织中CD66b的表达情况；在NACT第1个周期前行血常规检查，计数中性粒细胞及淋巴细胞，并计算NLR。采用χ2检验分析TANs和NLR与乳腺癌患者临床病理因素的相关性；采用单因素χ2检验和多因素logistic回归分析NACT疗效的影响因素；采用Kaplan-Meier生存分析和多因素Cox回归分析乳腺癌患者预后的影响因素；采用Spearman检验分析TANs与NLR的相关性。结果 CD66b在乳腺癌组织中的表达明显高于正常乳腺组织(P<0.001)，且弥漫性分布于肿瘤各处(癌巢和间质均可见浸润)。NACT前癌巢高浸润TANs与高临床分期、淋巴结转移和复发转移密切相关(P<0.05)；NACT前外周血高NLR与高cT分期和复发转移密切相关(P<0.05)。NACT前外周血NLR(P=0.007)、cT分期(P=0.041)、雌激素受体(ER)状态(P=0.009)和人表皮生长因子受体2(HER2)表达(P=0.020)是浸润性乳腺癌患者病理完全缓解(pCR)的独立预测因素。NACT前癌巢TANs(P=0.023)、高临床分期(P=0.040)、pCR(P=0.027)是影响浸润性乳腺癌患者无病生存期(DFS)的独立危险因素。NLR与TANs相关性不明显(r=0.14，P=0.071)。结论 NACT前癌巢内低浸润TANs预示乳腺癌患者预后更好；外周血高NLR与化疗耐药相关。

, correspAuthors=李淑琴, authorNote=null, correspAuthorsNote=
李淑琴，E-mail：
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林佳雯，硕士研究生，主要从事乳腺癌的临床研究

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林佳雯，硕士研究生，主要从事乳腺癌的临床研究

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林佳雯，硕士研究生，主要从事乳腺癌的临床研究

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J Clin Oncol, 2006, 24(11): 1656-1664., articleTitle=Estrogen-regulated genes predict survival in hormone receptor-positive breast cancers, refAbstract=null)], funds=null, companyList=[AuthorCompany(id=1198318893153481700, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, xref=1, ext=[AuthorCompanyExt(id=1198318893157676005, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, companyId=1198318893153481700, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1Department of Breast Surgery, Lianyungang Clinical Medical College, Nanjing Medical University, Lianyungang, Jiangsu 222000, China), AuthorCompanyExt(id=1198318893166064614, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, companyId=1198318893153481700, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1南京医科大学连云港临床医学院乳腺外科，江苏连云港 222000)]), AuthorCompany(id=1198318893241562089, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, xref=2, ext=[AuthorCompanyExt(id=1198318893245756394, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, companyId=1198318893241562089, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2Department of Breast Surgery, the First People Hospital of Lianyungang, Lianyungang, Jiangsu 222000, China), AuthorCompanyExt(id=1198318893254145003, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, companyId=1198318893241562089, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2连云港市第一人民医院乳腺外科，江苏连云港 222000)])], figs=[ArticleFig(id=1198318896336957542, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=EN, label=Fig.1, caption=Expression of CD66b in different tissues by immuno-histochemistry (HPF, ×200), figureFileSmall=Qj3HxE26UHEj60Do3EEhXw==, figureFileBig=gK4Iewq5ethiVhCoYfAteQ==, tableContent=null), ArticleFig(id=1198318896454398062, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=CN, label=图1, caption=CD66b在不同组织中表达的免疫组化染色结果(HPF, ×200)

黑色箭头示CD66b阳性表达；A. 正常乳腺组织(不表达)；B. 急性阑尾炎组织(阳性对照)；C. 乳腺癌癌巢(散在分布)；D. 乳腺癌间质(散在分布)

, figureFileSmall=Qj3HxE26UHEj60Do3EEhXw==, figureFileBig=gK4Iewq5ethiVhCoYfAteQ==, tableContent=null), ArticleFig(id=1198318896630558838, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=EN, label=Fig.2, caption=ROC curve of NLR in predicting pCR for invasive breast cancer, figureFileSmall=lUd3xXyNdgztFoCrI2LsjQ==, figureFileBig=n4sT3aA+z6eIQTZyfHeGEA==, tableContent=null), ArticleFig(id=1198318896714444923, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=CN, label=图2, caption=NLR预测浸润性乳腺癌pCR的ROC曲线

NLR. 中性粒细胞与淋巴细胞比值；pCR. 病理完全缓解

, figureFileSmall=lUd3xXyNdgztFoCrI2LsjQ==, figureFileBig=n4sT3aA+z6eIQTZyfHeGEA==, tableContent=null), ArticleFig(id=1198318896836079745, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=EN, label=Fig.3, caption=Multivariate logistic regression analysis of influencing factors of pCR in 167 patients with invasive breast cancer, figureFileSmall=GEYSSB9tTLiyxokrErllQQ==, figureFileBig=gPza4yGj6fQ9vfHFCjE+zQ==, tableContent=null), ArticleFig(id=1198318896911577222, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=CN, label=图3, caption=167例浸润性乳腺癌患者pCR影响因素的多因素logistic回归分析

pCR. 病理完全缓解；ER. 雌激素受体；PR. 孕激素受体；HER2. 人表皮生长因子受体2；NLR. 中性粒细胞与淋巴细胞比值；OR. 比值比

, figureFileSmall=GEYSSB9tTLiyxokrErllQQ==, figureFileBig=gPza4yGj6fQ9vfHFCjE+zQ==, tableContent=null), ArticleFig(id=1198318897008046219, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=EN, label=Fig.4, caption=Kaplan-Meier survival analysis of patients with invasive breast cancer, figureFileSmall=26aPKI/FRiHiI3h/SFnwQA==, figureFileBig=bMurrQDxfpRR1/Uuc/01sw==, tableContent=null), ArticleFig(id=1198318897100320913, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=CN, label=图4, caption=浸润性乳腺癌患者的Kaplan-Meier生存分析

TANs. 肿瘤相关中性粒细胞；NLR. 中性粒细胞与淋巴细胞比值；NACT. 新辅助化疗；DFS. 无病生存期

, figureFileSmall=26aPKI/FRiHiI3h/SFnwQA==, figureFileBig=bMurrQDxfpRR1/Uuc/01sw==, tableContent=null), ArticleFig(id=1198318897209372822, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=EN, label=Tab.1, caption=

The relationship between TANs, NLR and clinicopathologic factors in 167 patients with invasive breast cancer [n(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理因素 TANs NLR
低TANs组(n=83) 高TANs组(n=84) χ2 P 低NLR组(n=95) 高NLR组(n=72) χ2 P
年龄(岁) 1.010 0.315 3.115 0.078
>50 39(47.0) 46(54.8) 54(56.8) 31(43.1)
≤50 44(53.0) 38(45.2) 41(43.2) 41(56.9)
临床分期 5.298 0.021 1.456 0.228
Ⅱ 38(45.8) 24(28.6) 39(41.1) 23(31.9)
Ⅲ 45(54.2) 60(71.4) 56(58.9) 49(68.1)
cT分期 0.391 0.532 4.832 0.028
cT1+cT2 60(72.3) 57(67.9) 73(76.8) 44(61.1)
cT3+cT4 23(27.7) 27(32.1) 22(23.2) 28(38.9)
淋巴结转移 5.848 0.016 0.607 0.436
阳性 65(78.3) 77(91.7) 79(83.2) 63(87.5)
阴性 18(21.7) 7(8.3) 16(16.8) 9(12.5)
ER 0.288 0.592 0.158 0.691
阳性 47(56.6) 51(60.7) 57(60.0) 41(56.9)
阴性 36(43.4) 33(39.3) 38(40.0) 31(43.1)
PR 0.782 0.377 0.386 0.534
阳性 29(34.9) 24(28.6) 32(33.7) 21(29.2)
阴性 54(65.1) 60(71.4) 63(66.3) 51(70.8)
HER2 0.146 0.703 0.000 0.998
阳性 30(36.1) 28(33.3) 33(34.7) 25(34.7)
阴性 53(63.9) 56(66.7) 62(65.3) 47(65.3)
Ki-67 1.790 0.181 0.167 0.683
≥20% 64(77.1) 57(67.9) 70(73.7) 51(70.8)
<20% 19(22.9) 27(32.1) 25(26.3) 21(29.2)
分子分型 1.616 0.656 0.334 0.954
Luminal A 10(12.1) 7(8.4) 10(10.5) 7(9.7)
Luminal B 21(25.3) 28(33.3) 29(30.6) 20(27.8)
HER2阳性 30(36.1) 28(33.3) 33(34.7) 25(34.7)
TNBC 22(26.5) 21(25.0) 23(24.2) 20(27.8)
复发转移 7.716 0.005 6.096 0.014
是 8(9.6) 22(26.2) 11(11.6) 19(26.4)
否 75(90.4) 62(73.8) 84(88.4) 53(73.6)
), ArticleFig(id=1198318897335201948, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=CN, label=表1, caption=

167例浸润性乳腺癌患者TANs、NLR与临床病理因素的相关性[例(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理因素 TANs NLR
低TANs组(n=83) 高TANs组(n=84) χ2 P 低NLR组(n=95) 高NLR组(n=72) χ2 P
年龄(岁) 1.010 0.315 3.115 0.078
>50 39(47.0) 46(54.8) 54(56.8) 31(43.1)
≤50 44(53.0) 38(45.2) 41(43.2) 41(56.9)
临床分期 5.298 0.021 1.456 0.228
Ⅱ 38(45.8) 24(28.6) 39(41.1) 23(31.9)
Ⅲ 45(54.2) 60(71.4) 56(58.9) 49(68.1)
cT分期 0.391 0.532 4.832 0.028
cT1+cT2 60(72.3) 57(67.9) 73(76.8) 44(61.1)
cT3+cT4 23(27.7) 27(32.1) 22(23.2) 28(38.9)
淋巴结转移 5.848 0.016 0.607 0.436
阳性 65(78.3) 77(91.7) 79(83.2) 63(87.5)
阴性 18(21.7) 7(8.3) 16(16.8) 9(12.5)
ER 0.288 0.592 0.158 0.691
阳性 47(56.6) 51(60.7) 57(60.0) 41(56.9)
阴性 36(43.4) 33(39.3) 38(40.0) 31(43.1)
PR 0.782 0.377 0.386 0.534
阳性 29(34.9) 24(28.6) 32(33.7) 21(29.2)
阴性 54(65.1) 60(71.4) 63(66.3) 51(70.8)
HER2 0.146 0.703 0.000 0.998
阳性 30(36.1) 28(33.3) 33(34.7) 25(34.7)
阴性 53(63.9) 56(66.7) 62(65.3) 47(65.3)
Ki-67 1.790 0.181 0.167 0.683
≥20% 64(77.1) 57(67.9) 70(73.7) 51(70.8)
<20% 19(22.9) 27(32.1) 25(26.3) 21(29.2)
分子分型 1.616 0.656 0.334 0.954
Luminal A 10(12.1) 7(8.4) 10(10.5) 7(9.7)
Luminal B 21(25.3) 28(33.3) 29(30.6) 20(27.8)
HER2阳性 30(36.1) 28(33.3) 33(34.7) 25(34.7)
TNBC 22(26.5) 21(25.0) 23(24.2) 20(27.8)
复发转移 7.716 0.005 6.096 0.014
是 8(9.6) 22(26.2) 11(11.6) 19(26.4)
否 75(90.4) 62(73.8) 84(88.4) 53(73.6)
), ArticleFig(id=1198318897414893729, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=EN, label=Tab.2, caption=

Univariable analysis of influencing factors of pCR in 167 patients with invasive breast cancer [n(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
因素 非pCR(n=127) pCR(n=40) χ2 P
年龄(岁) 0.017 0.896
>50 65(51.2) 20(50.0)
≤50 62(48.8) 20(50.0)
临床分期 1.144 0.285
Ⅱ 50(39.4) 12(30.0)
Ⅲ 77(60.6) 28(70.0)
cT分期 3.881 0.049
cT1+cT2 84(66.1) 33(82.5)
cT3+cT4 43(33.9) 7(17.5)
淋巴结转移 1.045 0.307
阳性 110(86.7) 32(80.0)
阴性 17(13.3) 8(20.0)
ER 14.872 <0.001
阳性 85(66.9) 13(32.5)
阴性 42(33.1) 27(67.5)
PR 8.984 0.003
阳性 48(37.8) 5(12.5)
阴性 79(62.2) 35(87.5)
HER2 5.410 0.020
阳性 38(29.9) 20(50.0)
阴性 89(70.1) 20(50.0)
Ki-67 2.659 0.103
≥20% 88(69.3) 33(82.5)
<20% 39(30.7) 7(17.5)
TANs 0.591 0.442
高TANs 66(52.0) 18(45.0)
低TANs 61(48.0) 22(55.0)
NLR 7.037 0.008
高NLR 62(48.8) 10(25.0)
低NLR 65(51.2) 30(75.0)
), ArticleFig(id=1198318897507168424, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=CN, label=表2, caption=

167例浸润性乳腺癌患者pCR影响因素的单因素分析[例(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
因素 非pCR(n=127) pCR(n=40) χ2 P
年龄(岁) 0.017 0.896
>50 65(51.2) 20(50.0)
≤50 62(48.8) 20(50.0)
临床分期 1.144 0.285
Ⅱ 50(39.4) 12(30.0)
Ⅲ 77(60.6) 28(70.0)
cT分期 3.881 0.049
cT1+cT2 84(66.1) 33(82.5)
cT3+cT4 43(33.9) 7(17.5)
淋巴结转移 1.045 0.307
阳性 110(86.7) 32(80.0)
阴性 17(13.3) 8(20.0)
ER 14.872 <0.001
阳性 85(66.9) 13(32.5)
阴性 42(33.1) 27(67.5)
PR 8.984 0.003
阳性 48(37.8) 5(12.5)
阴性 79(62.2) 35(87.5)
HER2 5.410 0.020
阳性 38(29.9) 20(50.0)
阴性 89(70.1) 20(50.0)
Ki-67 2.659 0.103
≥20% 88(69.3) 33(82.5)
<20% 39(30.7) 7(17.5)
TANs 0.591 0.442
高TANs 66(52.0) 18(45.0)
低TANs 61(48.0) 22(55.0)
NLR 7.037 0.008
高NLR 62(48.8) 10(25.0)
低NLR 65(51.2) 30(75.0)
), ArticleFig(id=1198318897632997550, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=EN, label=Tab.3, caption=

Analysis of disease-free survival of 167 patients with invasive breast cancer

, figureFileSmall=null, figureFileBig=null, tableContent=
变量 P(1) HR(95%CI)(2) P(2)
年龄(>50岁 vs. ≤50岁) 0.143
临床分期(Ⅱ vs. Ⅲ) 0.033 0.308(0.100~0.947) 0.040
cT分期(cT1+cT2 vs. cT3+cT4) 0.032 0.825(0.378~1.803) 0.630
淋巴结状态(阳性 vs. 阴性) 0.608
ER(阳性 vs. 阴性) 0.550
PR(阳性 vs. 阴性) 0.654
HER2过表达(阳性 vs. 阴性) 0.970
Ki-67(<20% vs. ≥20%) 0.465
TANs(低TANs vs. 高TANs) 0.007 0.383(0.168~0.876) 0.023
NLR(低NLR vs. 高NLR) 0.019 0.627(0.292~1.345) 0.230
pCR(否 vs. 是) 0.006 9.814(1.305~73.805) 0.027
), ArticleFig(id=1198318897725272245, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=CN, label=表3, caption=

167例浸润性乳腺癌患者的无病生存分析结果

, figureFileSmall=null, figureFileBig=null, tableContent=
变量 P(1) HR(95%CI)(2) P(2)
年龄(>50岁 vs. ≤50岁) 0.143
临床分期(Ⅱ vs. Ⅲ) 0.033 0.308(0.100~0.947) 0.040
cT分期(cT1+cT2 vs. cT3+cT4) 0.032 0.825(0.378~1.803) 0.630
淋巴结状态(阳性 vs. 阴性) 0.608
ER(阳性 vs. 阴性) 0.550
PR(阳性 vs. 阴性) 0.654
HER2过表达(阳性 vs. 阴性) 0.970
Ki-67(<20% vs. ≥20%) 0.465
TANs(低TANs vs. 高TANs) 0.007 0.383(0.168~0.876) 0.023
NLR(低NLR vs. 高NLR) 0.019 0.627(0.292~1.345) 0.230
pCR(否 vs. 是) 0.006 9.814(1.305~73.805) 0.027
), ArticleFig(id=1198318897821741243, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=EN, label=Tab.4, caption=

The correlation between NLR and TANs of patients with invasive breast cancer [n(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
TANs NLR r P
高NLR(n=72) 低NLR(n=95)
高TANs(n=84) 42(58.3) 42(44.2) 0.14 0.071
低TANs(n=83) 30(41.7) 53(55.8)
), ArticleFig(id=1198318897960153283, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198196211661505132, language=CN, label=表4, caption=

浸润性乳腺癌患者NLR与TANs的相关性[例(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
TANs NLR r P
高NLR(n=72) 低NLR(n=95)
高TANs(n=84) 42(58.3) 42(44.2) 0.14 0.071
低TANs(n=83) 30(41.7) 53(55.8)
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肿瘤相关中性粒细胞和中性粒细胞与淋巴细胞比值对乳腺癌新辅助化疗疗效及预后的评估价值
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林佳雯 1 , 李淑琴 1, * , 卫姣飞 2
解放军医学杂志 | 临床研究 2024,49(12): 1386-1393
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解放军医学杂志 | 临床研究 2024, 49(12): 1386-1393
肿瘤相关中性粒细胞和中性粒细胞与淋巴细胞比值对乳腺癌新辅助化疗疗效及预后的评估价值
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林佳雯1, 李淑琴1, * , 卫姣飞2
作者信息
  • 1南京医科大学连云港临床医学院乳腺外科，江苏连云港 222000
  • 2连云港市第一人民医院乳腺外科，江苏连云港 222000

    • 林佳雯，硕士研究生，主要从事乳腺癌的临床研究

通讯作者:

李淑琴，E-mail：
The value of tumor associated neutrophils and neutrophil to lymphocyte ratio in evaluating the efficacy and prognosis of neoadjuvant chemotherapy for breast cancer
Jia-Wen Lin1, Shu-Qin Li1, * , Jiao-Fei Wei2
Affiliations
  • 1Department of Breast Surgery, Lianyungang Clinical Medical College, Nanjing Medical University, Lianyungang, Jiangsu 222000, China
  • 2Department of Breast Surgery, the First People Hospital of Lianyungang, Lianyungang, Jiangsu 222000, China
出版时间: 2024-12-28 doi: 10.11855/j.issn.0577-7402.0574.2023.0911
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摘要
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目的 探讨CD66b+ 肿瘤相关中性粒细胞(TANs)和中性粒细胞与淋巴细胞比值(NLR)对乳腺癌新辅助化疗(NACT)疗效及预后的评估价值。方法 回顾性收集2015年1月－2020年6月在连云港市第一人民医院乳腺外科接受NACT治疗的167例浸润性乳腺癌患者的乳腺癌组织，同时收集正常乳腺组织40例作为对照。采用免疫组化染色检测NACT前乳腺癌组织和正常乳腺组织中CD66b的表达情况；在NACT第1个周期前行血常规检查，计数中性粒细胞及淋巴细胞，并计算NLR。采用χ2检验分析TANs和NLR与乳腺癌患者临床病理因素的相关性；采用单因素χ2检验和多因素logistic回归分析NACT疗效的影响因素；采用Kaplan-Meier生存分析和多因素Cox回归分析乳腺癌患者预后的影响因素；采用Spearman检验分析TANs与NLR的相关性。结果 CD66b在乳腺癌组织中的表达明显高于正常乳腺组织(P<0.001)，且弥漫性分布于肿瘤各处(癌巢和间质均可见浸润)。NACT前癌巢高浸润TANs与高临床分期、淋巴结转移和复发转移密切相关(P<0.05)；NACT前外周血高NLR与高cT分期和复发转移密切相关(P<0.05)。NACT前外周血NLR(P=0.007)、cT分期(P=0.041)、雌激素受体(ER)状态(P=0.009)和人表皮生长因子受体2(HER2)表达(P=0.020)是浸润性乳腺癌患者病理完全缓解(pCR)的独立预测因素。NACT前癌巢TANs(P=0.023)、高临床分期(P=0.040)、pCR(P=0.027)是影响浸润性乳腺癌患者无病生存期(DFS)的独立危险因素。NLR与TANs相关性不明显(r=0.14，P=0.071)。结论 NACT前癌巢内低浸润TANs预示乳腺癌患者预后更好；外周血高NLR与化疗耐药相关。

乳腺癌  /  新辅助化疗  /  肿瘤相关中性粒细胞  /  中性粒细胞与淋巴细胞比值  /  病理完全缓解

Objective To investigate the value of CD66b+ tumor-associated neutrophils (TANs) and neutrophil to lymphocyte ratio (NLR) in evaluating the efficacy and prognosis of neoadjuvant chemotherapy (NACT) for breast cancer. Methods One hundred and sixty-seven patients of invasive breast cancer treated with NACT in the Department of Breast Surgery, the First People Hospital of Lianyungang from January 2015 to June 2020 were collected, and 40 cases of normal breast tissues were collected. Immunohistochemistry was used to detect the expression of CD66b in breast cancer tissues before NACT and normal breast tissues. Peripheral venous blood was taken from patients within 1 week before the first cycle of NACT, count neutrophils and lymphocytes were counted and their ratio (NLR) was calculated. The correlation between TANs and NLR and clinicopathologic features was analyzed by χ2 test. The influencing factors of efficacy of NACT were analyzed by univariate χ2 test and multivariate logistic analysis. Kaplan-Meier survival analysis and multivariate Cox analysis were used to determine the prognostic factors. The correlation between TANs and NLR was determined by Spearman test. Results The expression of CD66b in breast cancer tissues was significantly higher than that in normal breast tissues (P<0.05), and it was diffusely distributed throughout the tumor (cancer nest and stroma were infiltrated). High infiltration of parenchymal TANs before NACT was correlated with high clinical stage, lymph node metastasis, and recurrence and metastasis (P<0.05). High NLR before NACT was closely related to high cT stage and recurrence and metastasis (P<0.05). NLR of peripheral blood (P=0.007), cT stage (P=0.041), estrogen receptor (ER) status (P=0.009), and human epidermal growth factor 2 (HER2) expression (P=0.020) were independent predictors for pathologic complete response (pCR). TANs (P=0.023), high clinical stage (P=0.040), and pCR (P=0.027) before NACT were independent risk factors for disease-free survival (DFS) of patients with invasive breast cancer. There was no correlation between NLR and TANs (r=0.14, P=0.071). Conclusions Low infiltration of parenchymal TANs before NACT predicts a better prognosis for patients with breast cancer. Higher NLR in peripheral blood is associated with chemotherapy resistance.

breast cancer  /  neoadjuvant chemotherapy  /  tumor-associated neutrophils  /  neutrophil to lymphocyte ratio  /  pathologic complete response
林佳雯, 李淑琴, 卫姣飞. 肿瘤相关中性粒细胞和中性粒细胞与淋巴细胞比值对乳腺癌新辅助化疗疗效及预后的评估价值. 解放军医学杂志, 2024 , 49 (12) : 1386 -1393 . DOI: 10.11855/j.issn.0577-7402.0574.2023.0911
Jia-Wen Lin, Shu-Qin Li, Jiao-Fei Wei. The value of tumor associated neutrophils and neutrophil to lymphocyte ratio in evaluating the efficacy and prognosis of neoadjuvant chemotherapy for breast cancer[J]. Medical Journal of Chinese People’s Liberation Army, 2024 , 49 (12) : 1386 -1393 . DOI: 10.11855/j.issn.0577-7402.0574.2023.0911
正文
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2020年乳腺癌的发病率居全球癌症第1位[1]。目前，新辅助化疗(neoadjuvant chemotherapy，NACT)已被广泛用于乳腺癌的综合治疗中[2]。NACT的病理完全缓解(pathologic complete response，pCR)定义为乳腺原发灶和腋窝没有残留浸润癌(伴或不伴原位癌)，与改善患者长期生存结果密切相关。多项研究显示，与未获得pCR的乳腺癌患者相比，获得pCR患者的无病生存期(disease free survival，DFS)及总生存期(overall survival，OS)均显著改善，尤其是三阴性乳腺癌(triple-negative breast cancers，TNBC)、人表皮生长因子受体2(human epidermal growth factor receptor 2，HER2)阳性乳腺癌及激素受体阴性乳腺癌患者[3-5]。然而，并非所有患者均可获得pCR。部分患者对NACT耐药，甚至治疗期间即发生疾病进展。因此，在开始NACT前权衡治疗的风险和益处，寻找可靠的指标对乳腺癌NACT的化疗反应进行预测具有一定的临床意义。肿瘤相关中性粒细胞(tumour-associated neutrophils，TANs)是肿瘤局部炎症反应的重要组成部分，中性粒细胞与淋巴细胞比值(neutrophil to lymphocyte ratio，NLR)是反映全身炎症和宿主免疫反应的重要指标[6]，监测全身和局部免疫状态可能反映乳腺癌患者的化疗疗效和预后。目前，TANs、NLR与NACT疗效及预后的相关性尚存在争议，且TANs与NLR相关性的研究鲜少。本研究探讨NLR与TANs的相关性及两者对NACT疗效及预后的影响。
1 资料与方法
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1.1 研究对象
回顾性选取2015年1月－2020年6月在连云港市第一人民医院乳腺外科行病理活检诊断为浸润性乳腺癌的167例患者，收集其NACT前乳腺癌组织标本。同时，选取2020年1－6月于该院诊断为乳腺纤维瘤或乳腺腺病的40例患者，收集其周围正常乳腺组织标本作为对照，所有标本经固定后石蜡包埋。纳入标准：(1)穿刺活检组织学证实为浸润性乳腺癌并诊断为Ⅱ、Ⅲ期；(2)NACT前未进行其他抗肿瘤治疗，确诊后接受≥4个NACT周期，且NACT后行乳腺癌根治性手术或保乳手术；(3)在NACT第1个周期前行血常规检查。排除标准：(1)转移乳腺癌、炎性乳腺癌、男性乳腺癌、双侧乳腺癌及其他恶性肿瘤史；(2)急慢性炎症和血液系统疾病；(3)血常规、免疫组化染色等结果缺失，病例资料不完整。本研究经连云港市第一人民医院伦理委员会批准(KY-20221209001-1)。
1.2 方法
1.2.1 CD66b+ TANs检测
采用免疫组化染色检测乳腺癌组织和正常乳腺组织中CD66b的表达情况。将石蜡包埋组织块切成2 μm的切片，于二甲苯溶液中脱蜡，水合。抗原修复后用过氧化氢溶液抑制内源性过氧化物酶。滴加兔抗人CD66b单克隆抗体(1:2000稀释；ab300122，英国Abcam公司) 37 ℃孵育过夜；滴加二抗37 ℃孵育30 min；滴加DAB显色液，显微镜观察至发现棕色后，用苏木精染色1 min，脱水封片，200倍显微镜下观察。以富含TANs的急性阑尾炎组织作为阳性对照，PBS缓冲液代替一抗作为阴性对照。阳性结果判断：CD66b阳性染色为定位于细胞膜的棕色颗粒。乳腺癌组织和正常乳腺组织切片经过CD66b染色后，采用数字化病理切片扫描系统扫描采集高清晰度染色图像。每张切片随机选择5个高倍视野(HPF，×200)，计数癌巢内TANs的总数作为其密度。CD66b免疫染色的评价由两名对临床资料完全不知情的病理学家独立进行，以中位数区分TANs高、低密度。
1.2.2 NLR检测及最佳截断值判定
浸润性乳腺癌患者在接受NACT第1个周期前1周内采集空腹前臂外周静脉血4 ml，经抗凝处理，分别计数中性粒细胞和淋巴细胞，4 h内完成检测，并计算NLR。NLR=绝对中性粒细胞计数/绝对淋巴细胞计数。所有血细胞评估均在连云港市第一人民医院实验室根据标准化手术程序集中进行。采用受试者工作特征(receiver operating characteristic，ROC)曲线确定NLR的最佳截断值，以pCR为终点检验变量生成ROC曲线，曲线下面积(area under curve，AUC)最大的点所对应的值作为截断值区分NLR高、低值。
1.2.3 病理检测
采用免疫组化染色和FISH法检测乳腺癌组织中雌激素受体(estrogen receptor，ER)、孕激素受体(progesterone receptor，PR)、HER2和Ki-67的表达情况。参考2013年St Gallen会议和2020版ASCO指南，ER和PR阳性定义为浸润性肿瘤细胞核着色≥1%，HER2阳性定义为免疫组化染色(+++)或FISH检测阳性，Ki-67阳性定义为Ki-67≥20%。
1.2.4 疗效评价
根据美国癌症联合会(American Joint Committee on Cancer，AJCC)第8版，pCR定义为NACT后手术标本中原发部位/腋窝淋巴结中无浸润性乳腺癌(ypT0/ypTis，ypN0)，允许非浸润性乳腺癌残留(导管原位癌)。
1.3 随访
术后2年内每3个月随访1次，5年内每6个月随访1次，此后1年随访1次。起始时间为手术日，截止时间为2023年1月。每次随访均进行血常规、胸部CT、肿瘤标志物、乳房、肝胆胰脾等超声检查。骨痛患者进行骨扫描。DFS定义为复发者确诊至复发的时间间隔，或未复发者确诊至最后一次随访的时间间隔。复发定义为局部或远处出现既往肿瘤(通过临床、放射学或病理诊断)。
1.4 指标分析
(1)TANs、NLR与浸润性乳腺癌患者临床病理因素的相关性；(2)NACT疗效的影响因素；(3)浸润性乳腺癌患者预后的影响因素；(4)TANs与NLR的相关性。
1.5 统计学处理
采用SPSS 27.0软件进行统计分析，GraphPad Prism和Adobe Photoshop软件作图。所有数据均为计数资料，以率(%)表示，组间比较采用χ2检验或Fisher确切概率法。采用χ2检验分析TANs、NLR与浸润性乳腺癌临床病理因素的相关性。采用单因素χ2检验和多因素logistic回归分析NACT疗效的影响因素。Kaplan-Meier生存分析和多因素Cox回归分析浸润性乳腺癌患者预后的影响因素。采用Spearman检验分析TANs与NLR的相关性。对有意义的因子使用共线性检验检测多重共线性(方差膨胀因子<10表明多重共线性不显著)。P<0.05为差异有统计学意义。
2 结果
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2.1 一般情况
共纳入167例浸润性乳腺癌患者，确诊时中位年龄51(26~77)岁；均为浸润性导管癌；临床分期以Ⅲ期为主(62.9%，105/167)；肿瘤大小以cT1和cT2为主(70.1%，117/167)。ER阳性占58.7%(98/167)；PR阳性占31.7%(53/167)；HER2阳性占34.7%(58/167)；Ki-67阳性占72.5%(121/167)。术后病理证实24.0%(40/167)的患者获得pCR。
2.2 CD66b+ TANs浸润情况
免疫组化染色结果显示，CD66b在正常乳腺组织中不表达，在乳腺癌组织中呈不同程度的表达(图1)。CD66b在正常乳腺组织和乳腺癌组织中的阳性表达率分别为0%和86.8%，差异有统计学意义(P<0.001)。乳腺癌组织中CD66b阳性染色弥漫性分布于肿瘤各处，癌巢和间质内均可见CD66b+ TANs浸润(图1)。NACT前癌巢内TANs浸润密度为0~150个/5HPF，中位数为9个/5HPF，均数为14.53个/5HPF。根据TANs的中位数将患者分为高TANs组(n=84)与低TANs组(n=83)。
2.3 NACT前NLR对浸润性乳腺癌pCR的预测价值
ROC曲线分析结果显示，NACT前外周血NLR预测浸润性乳腺癌pCR的最佳截断值为2.20，特异度为75.0%，敏感度为48.8%，差异均有统计学意义(AUC=0.630，95%CI 0.528~0.732，P=0.013，图2)。
依据NLR预测浸润性乳腺癌pCR的最佳截断值将患者分为高NLR组(n=72)与低NLR组(n=95)。
2.4 TANs、NLR与浸润性乳腺癌患者临床病理因素的相关性
NACT前癌巢高浸润TANs与高临床分期(P=0.021)、淋巴结转移(P=0.016)和复发转移(P=0.005)密切相关，而年龄、cT分期、ER状态、PR状态、HER2表达、Ki-67状态和分子分型在不同TANs之间无明显差异(P>0.05)。NACT前高NLR与高cT分期(P=0.028)和复发转移(P=0.014)密切相关，与其他因素无关(P>0.05) (表1)。
2.5 浸润性乳腺癌患者NACT疗效的影响因素分析
单因素分析结果显示，NACT前外周血cT分期(P=0.049)、ER状态(P<0.001)、PR状态(P=0.003)、HER2表达(P=0.020)、NLR(P=0.008)与浸润性乳腺癌患者的pCR有关。低NLR患者的pCR率明显高于高NLR患者[31.6%(30/95) vs. 13.9%(10/72)，χ2=7.037，P=0.008]。年龄、临床分期、淋巴结转移、Ki-67、TANs与pCR状态无关(P>0.05，表2)。
以是否获得pCR(否=0，是=1)为因变量，以NLR(高NLR=0，低NLR=1)、cT分期(cT3+cT4=0，cT1+cT2=1)、ER状态(ER阳性=0，ER阴性=1)、PR状态(PR阳性=0，PR阴性=1)、HER2表达(HER2高表达=0，HER2低表达=1)为自变量进行多因素logistic回归分析，结果显示，cT分期(P=0.041)、ER状态(P=0.009)、HER2表达(P=0.020)、NLR(P=0.007)是pCR的独立预测因素，而PR状态(P=0.258)与pCR无关(图3)。
2.6 浸润性乳腺癌患者预后的影响因素分析
167例浸润性乳腺癌患者随访时间为46.8(6~92)个月，其中30例(18.0%)在随访期间复发转移。Kaplan-Meier生存分析结果显示，NACT前癌巢TANs(P=0.007)、NLR(P=0.019)、临床分期(P=0.033)、cT分期(P=0.032)以及是否获得pCR(P=0.006)为浸润性乳腺癌患者DFS的影响因素(表3，图4)。
以是否发生复发转移(否=0，是=1)为因变量，以生存时间为时间变量，以TANs(高TANs=0，低TANs=1)、NLR(高NLR=0，低NLR=1)、临床分期(Ⅲ期=0，Ⅱ期=1)、cT分期(cT3+cT4=0，cT1+cT2=1)和pCR(pCR=0，非pCR=1)为自变量进行多因素Cox回归分析，结果显示，高临床分期(HR=0.308，95%CI 0.100~0.947，P=0.040)、癌巢TANs(HR=0.383，95%CI 0.168~0.876，P=0.023)、pCR(HR=9.814，95%CI 1.305~73.805，P=0.027)是影响浸润性乳腺癌患者DFS的独立危险因素(表3)。
2.7 浸润性乳腺癌患者TANs与NLR的相关性
Spearman检验结果显示，浸润性乳腺癌患者的TANs与NLR无相关性(r=0.14，P=0.071，表4)。
3 讨论
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炎症性疾病可能增加肿瘤发生、进展及转移的风险[7]。肿瘤相关炎症包括局部和全身炎症反应，研究慢性炎症局部和全身标志物对恶性肿瘤的诊断、治疗、疗效评估和预后预测至关重要。TANs是肿瘤局部炎症反应的重要组成部分。越来越多的证据表明，TANs能够通过促进血管生成，刺激肿瘤细胞的迁移和侵袭，以及调节其他免疫细胞作为“免疫抑制开关”的一部分来促进肿瘤进展[8]。有研究表明，TANs在乳腺癌微环境中浸润数量很少，与pCR和预后无关[9]。但也有研究发现，乳腺癌中存在大量TANs浸润，且与复发转移有关[10-11]。本研究结果显示，CD66b在乳腺癌组织中的表达明显高于正常乳腺组织，癌巢和间质内均可见CD66b+ TANs浸润。研究发现，与瘤周和间质TANs比较，癌巢内TANs被证实与不良预后明显相关[12]。本研究主要分析癌巢内TANs，发现癌巢TANs在不同临床分期、淋巴结转移和复发转移乳腺癌患者中存在差异，且癌巢内高浸润CD66b+ TANs被证实为乳腺癌患者不良预后的独立危险因素。高临床分期、淋巴结转移和复发转移表明肿瘤进展，提示癌巢TANs与乳腺癌的侵袭性密切相关，且与较差的生存预后有关。但高、低TANs组患者的pCR率无明显差异，尚需进一步扩大样本量来证实TANs与pCR的关系。
NLR是反映全身炎症和宿主免疫反应的重要指标，代表着促瘤炎症状态与抗瘤免疫状态之间的平衡。NLR升高表明平衡倾向于促肿瘤炎症。近年来，NLR已被证实是预测各种癌症预后的有效指标[13]。Ethier等[14]纳入15项研究(包括8563例乳腺癌患者)进行Mata分析，发现在乳腺癌患者中，尤其是在TNBC和HER2阳性乳腺癌患者中，高NLR与较差的OS和DFS相关。而NLR是否可作为NACT疗效的预测指标仍存在争议。Graziano等[15]发现，低NLR可能表明免疫系统处于激活状态。2021年，Zhu等[16]回顾性分析了346例乳腺癌患者的临床资料，发现较高的NLR与较低的pCR率相关，NLR可作为NACT后pCR的独立预测因素。而Eryilmaz等[17]发现，pCR与NLR无关，可能的原因为目前对于NLR的分界值尚无统一标准，部分研究使用ROC曲线来确定NLR的界值，如Graziano等[15]、Zhu等[16]和Chen等[18]发现NLR的截断值分别为2.42、1.695、2.06，而另有部分研究使用中位数或平均值作为NLR高低的分界值[19-20]。
本研究使用ROC曲线确定NACT前NLR的截断值为2.20。进一步分析显示，低NLR乳腺癌患者的pCR率明显高于高NLR患者，高NLR患者对NACT反应较差，与Zhu等[16]的研究结果一致。由此可见，NLR值越低的患者越有可能达到pCR。有研究发现，肿瘤直径和复发转移与NLR呈正相关，提示NLR升高可能与化疗耐药有关[11]。既往研究发现，肿瘤直径越大的患者获得pCR的可能性越小[21-22]。此外，本研究单因素分析结果显示，NLR是影响乳腺癌患者预后的危险因素，但在多因素Cox回归分析中，NLR与预后无关，这可能与随访时间不足或样本量较少有关。
在乳腺癌的治疗过程中，监测患者的炎症状态是必不可少的。在细菌感染的情况下，全身炎症反应通常与感染的严重程度相关。而全身炎症与局部炎症之间的关系尚不完全清楚。笔者推测肿瘤局部炎症可能影响全身炎症状态。为了验证这一假设，本研究选择外周血NLR和癌巢TANs分别代表全身和局部免疫状态，发现NLR与TANs之间无相关性(P>0.05)。分析原因可能为获得的石蜡病理标本较少，或其他全身和局部炎症标志物对外周血NLR与癌巢TANs之间的相关性有干扰。目前尚不能得出NLR与TANs浸润程度之间的关系。
既往研究发现，肿瘤直径≤5 cm、淋巴结阴性、ER阴性、PR阴性、HER2过表达、Ki-67高表达以及非Luminal型乳腺癌与更高的pCR率相关[4,21,23-25]。本研究发现，cT分期、ER状态、HER2表达是pCR的独立预测因素，与既往研究结果相符。此外，本研究还发现，高临床分期和pCR是影响DFS的独立危险因素。既往研究发现，乳腺癌的预后受多种因素影响，包括肿瘤大小和淋巴结受累等形态指标，以及激素受体、Ki-67、HER2和分子分型等生物学指标[26-28]。多项研究显示，pCR与乳腺癌患者良好的预后相关[3]。pCR通常标志着预后的改善，被视为长期生存的替代终点。本研究中，低临床分期和pCR患者的预后明显改善，与既往报道一致[22]。但本研究未发现肿瘤大小、激素受体等其他因素与乳腺癌预后的相关性，尚需扩大样本量进一步研究。
综上所述，NACT前癌巢内低浸润TANs预示着乳腺癌患者具有更好的预后；外周血高NLR与化疗耐药相关，但NLR与TANs相关性不明显。但本研究具有一定局限性：(1)为单中心回顾性分析，病例数量和可获得的乳腺癌石蜡标本较少；(2)不能完全排除个体或外界因素对外周血数据准确性的影响；(3)仅研究了癌巢TANs，间质TANs在乳腺癌中的作用仍需进一步分析；(4)缺乏对肿瘤浸润淋巴细胞(tumor infiltrating lymphocytes，TILs)的评估，TANs/TIL或许较TANs更具代表性，尚需要进一步研究来验证局部与全身炎症反应的关系。未来可控制混杂因素，继续深入开展大样本的前瞻性、多中心研究。
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2024年第49卷第12期
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doi: 10.11855/j.issn.0577-7402.0574.2023.0911
  • 接收时间：2023-04-19
  • 首发时间：2025-11-20
  • 出版时间：2024-12-28
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  • 收稿日期：2023-04-19
  • 录用日期：2023-05-18
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    1南京医科大学连云港临床医学院乳腺外科，江苏连云港 222000
    2连云港市第一人民医院乳腺外科，江苏连云港 222000

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鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
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红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
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