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. 2015 Mar 26;9(6):2825–2832. doi: 10.3892/ol.2015.3072

Effect of neoadjuvant chemotherapy in patients with triple-negative breast cancer: A meta-analysis

MUYOU TIAN 1,2, YAHUA ZHONG 1,2, FUXIANG ZHOU 1,2, CONGHUA XIE 1,2, YUNFENG ZHOU 1,2, ZHENGKAI LIAO 1,2,✉
PMCID: PMC4473711  PMID: 26137155

Abstract

The present meta-analysis aimed to evaluate the effect of neoadjuvant chemotherapy on pathological complete response (pCR) and survival rate in patients with triple-negative breast cancer (TNBC). Specific inclusion and exclusion criteria were used to conduct a search of the available databases, in order to find studies performed between January 2006 and January 2014. The bibliographies of the included studies were examined with the same criteria. The Grading of Recommendations Assessment, Development and Evaluation (GRADE) working group framework was used to evaluate the included studies, and RevMan 5.1 and GRADEprofiler 3.6 were used to analyze the extracted data. A total of 19 studies with 6,180 patients were included. The meta-analysis revealed that the pCR rates in patients with TNBC were significantly higher than those in patients with non-TNBC. The 5-year disease-free survival (DFS) and overall survival (OS) rates were significantly lower in the patients with TNBC compared with those with non-TNBC. Furthermore, these survival rates were significantly higher in the patients with TNBC who achieved a pCR compared with those in the patients who did not achieve a pCR. pCR rates were higher among the patients with TNBC with high Ki-67 expression than among those with low Ki-67 expression. The patients with TNBC exhibited lower survival rates compared with those with non-TNBC, but achieved higher pCR rates. Moreover, those patients achieving a pCR exhibited improved 5-year survival rates, suggesting that the pCR rate could be predictive of survival in patients with TNBC. In addition, high Ki-67 expression may predict the likelihood of a pCR. However, future multicenter randomized controlled trials are required to enhance the quantity and quality of the clinical evidence.

Keywords: triple-negative breast cancer, neoadjuvant chemotherapy, pathological complete response, survival, molecular marker

Introduction

Breast cancer is subdivided into five types, namely luminal A, luminal B, human epidermal growth factor receptor-2 (HER-2)-positive, normal-like and basal-like breast cancer, according to cellular-molecular phenotype (1). In total, ∼90% of triple-negative breast cancer (TNBC) cases are classified as basal-like. TNBC, as its name suggests, has an estrogen receptor (ER)-negative, progesterone receptor (PR)-negative and HER-2-negative phenotype, and accounts for 15% of all breast cancer cases. TNBC is highly aggressive, with a high propensity for metastasis and a poor survival rate (2,3). Therefore, endocrine and molecularly targeted therapies are unsuitable for patients with TNBC, and chemotherapy is the only systemic therapy available.

Neoadjuvant chemotherapy (NAC) has become a widely applied treatment for early-stage breast cancer (4). NAC can downstage a tumor, potentially enabling breast-conserving surgery for patients who may have otherwise required mastectomy (5,6). Based on preclinical studies in animal models, it was hypothesized that NAC may diminish the micrometastases of breast cancer (7). In general, tumor size and lymph node number are the foremost prognostic predictors of solid tumors following systemic therapy, but they are not appropriate for determining the response to NAC. A pathological complete response (pCR) is used as a short-term evaluation index for the efficacy of NAC.

Patients with TNBC usually achieve a higher pCR rate (8,9). Furthermore, it has been reported that patients with TNBC and those with non-TNBC who achieved pCR following NAC have similar long-term survival rates. By contrast, the 5-year disease-free survival (DFS) rates of patients who did not achieve pCR following NAC differed significantly between those patients with TNBC and those with non-TNBC (10). However, a meta-analysis in 2011 reported that pCR is an independent prognostic factor of overall survival (OS), DFS and relapse-free survival (RFS) for patients with TNBC (11). Other studies indicated that molecular biomarkers, including Ki-67 antigen, tumor suppressor p53, epidermal growth factor receptor (EGFR), and cytokeratin (CK)5 and 6, may predict the pCR rate of patients with TNBC following NAC (12,13).

In this meta-analysis, data was extracted and the short-term efficacy (pCR) and long-term survival (DFS and OS) rates of patients with TNBC treated with NAC were analyzed. In order to provide prognostic guidance for TNBC patients, the present meta-analysis attempted to further prove the association between pCR and long-term survival, and to determine if any biomarkers were predictive of the pCR rate.

Materials and methods

Inclusion and exclusion criteria

Prospective or retrospective controlled trials were included, regardless of the allocation, concealment or blinding. All the following criteria had to be met for inclusion in the meta-analysis: i) NAC must have been the primary initial therapy; ii) patients must have had stage I-III breast cancer; iii) immunohistochemical staining should have confirmed hormone receptor status and/or fluorescence in situ hybridization should have confirmed HER-2 status; and iv) the pCR rate, and DFS or OS rates had to have been reported. Studies were excluded if they met any of the following criteria: i) Repetitive publication; ii) small sample size; iii) abstract only; and iv) no sufficient raw data and data unavailable on request.

Literature search strategy

TNBC is a concept that was initially introduced in 2006 (14); therefore, searches of the PubMed database, the China Knowledge Resource Integrated Database, the China Science and Technology Journal Database, and the WanFang database were performed using date limits of between January 2006 and January 2014. Papers in the Chinese and English languages were searched. Retrieval keywords included i) triple-negative breast cancer or TNBC; ii) neoadjuvant chemotherapy or NAC; iii) pathological complete response or pCR; iv) survival or disease-free survival or DFS or overall survival or OS; v) molecular marker or CK5/6 or p53 or Ki-67; and vi) combinations of these terms, including i)+ii), i)+ii)+iii), i)+ii)+iv) and i)+ii)+v).

Data extraction

Based on the aforementioned strategies, studies were selected and their eligibility was confirmed by three independent researchers. The following information was extracted from each study: Authors' names, year of publication, study type, total number of patients, median patient age, primary tumor-node-metastasis (TNM) stage, NAC regimen and survival data.

Quality evaluation

The Grading of Recommendations Assessment, Development and Evaluation (GRADE) working group framework was used to evaluate the collated data; accordingly, high, medium, low or very low grades were awarded with regard to quality. Randomized controlled trials were considered to be of a high grade, but the following factors were also considered: Risk of bias, indirectness, inconsistency, imprecision and publication bias. Case-control and cohort studies were considered to be of a medium grade.

Statistical analyses

Review Manager software (RevMan, version 5.1 for Windows; The Cochrane Collaboration, Oxford, UK) was used to conduct the meta-analysis. Odds ratio (OR) and 95% confidence interval (95% CI) values were calculated. A χ2 test was used to evaluate heterogeneity in the data. The fixed-effects model was used for studies without significant heterogeneity (I2≤50% or P≥0.10), whereas the random-effects model was used for studies with significant heterogeneity. Funnel plots were generated using RevMan to detect publication bias. GRADEpro software (version 3.6 for Windows; The Cochrane Collaboration) was used to conduct the quality evaluation.

Results

Eligible studies and data summary

A total of 480 studies were first identified for evaluation. Based on the criteria described in the methods, 19 publications were eligible for inclusion in the present meta-analysis (10,12,15–31). The bibliographies of these 19 publications were also searched, but this did not provide further studies for inclusion. Therefore, a final total of 19 studies with 6,180 patients were included. The search process is described in Fig. 1. The anthracycline-based and/or paclitaxel regimens were the most common NAC regimens applied. Table I describes the characteristics of the eligible studies in more detail.

Figure 1.

Figure 1.

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Flow-chart of the literature search process. CNKI, China Knowledge Resource Integrated database; VIP, China Science and Technology Journal database.

Table I.

Characteristics of eligible studies.

First author, year (ref.) Study types Total patients, n Median age, years Stages NAC regimensa
Bidard et al, 2008 (18) Retrospective 293 50 I-III FEC or FAC x(4–6)
Chang et al, 2010 (19) Prospective 74 49 II-III TC ×4
Darb-Esfahani et al, 2009 (20) Prospective 913 - II-III AT ×4, or AC ×4 + docetaxel ×4
Fisher et al, 2012 (21) Retrospective 385 50 I-III -
Frasci et al, 2009 (22) Prospective 74 48 II-III AT+cisplatin ×8
Medioni et al, 2011 (27) Prospective 74 50 II-III Docetaxel+gemcitabine ×2, or vinorelbine+epirubicin ×2
Keam et al, 2011 (23) Prospective 105 - II-III Docetaxel or Adriamycin ×3
Li et al, 2011 (24) Retrospective 316 50 I-III CAF+taxanes
Li et al, 2011 (12) Prospective 220 48 II-III AT x(4–6)
Liedtke et al, 2008 (25) Prospective 1118 48 I-III FAC/FEC/AC, or TFAC/TFEC, or Single-agent taxane
Masuda et al, 2011 (26) Prospective 163 50 I-III FEC ×4, or AT ×4
Ono et al, 2012 (28) Prospective 474 53 II-III AC/AT/CEF
Tang et al, 2012 (29) Retrospective 198 - I-III CEF/CMF/paclitaxel
Wu et al, 2011 (30) Retrospective 249 47 II-III AT ×4
Yoo et al, 2012 (31) Retrospective 276 44 I-III -
Jia et al, 2012 (17) Retrospective 249 47 II-III ET
Sun et al, 2009 (15) Prospective 326 47 II-III CTF ×4
Wang and Gao, 2010 (16) Retrospective 535 45 I-III FEC ×4
Zhou et al, 2009 (10) Retrospective 138 51 II-III AT ×4
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a

‘x’ indicates number of cycles (e.g. ×4, four cycles). FEC, cyclophosphamide+epirubicin+fluorouracil; FAC, cyclophosphamide+Adriamycin+fluorouracil; TC, docetaxel+cyclophosphamide; AT, Adriamycin+docetaxel; ET, epirubicin+docetaxel; AC, Adriamycin+docetaxel; CAF, cyclophosphamide+Adriamycin+fluorouracil; CEF, cyclophosphamide+epirubicin+fluorouracil; CTF, cyclophosphamide+docetaxel+fluorouracil; TFAC, docetaxel+FAC; TFEC, docetaxel+FEC.

pCR in patients with TNBC and non-TNBC

A total of 13 studies (10,15–20,24,25,27–30) reported the pCR rates in patients with TNBC and non-TNBC who received NAC. There was no heterogeneity between the results of different studies (I2=23%, P=0.21), so the fixed-effects model was applied for data analysis. The pCR rates in the patients with TNBC were significantly higher than those in the patients with non-TNBC (OR, 3.10; 95% CI, 2.51–3.82; Fig. 2).

Figure 2.

Figure 2.

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Forest plot: Pathological complete response rate in patients with TNBC and non-TNBC who received neoadjuvant chemotherapy. TNBC, triple-negative breast cancer; CI, confidence interval.

Survival in patients with TNBC and non-TNBC

A total of 6 studies (10,16,17,24,25,30) reported the 5-year DFS rate in patients with TNBC or non-TNBC who received NAC. There was significant heterogeneity between the different research results (I2=65%, P=0.01), so the random-effects model was applied for data analysis. The 5-year DFS rate in the patients with TNBC was significantly lower than that in the patients with non-TNBC (54.6 vs. 70.8%; OR, 0.53; 95% CI, 0.34–0.81; Fig. 3).

Figure 3.

Figure 3.

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Forest plot: 5-year diseasae-free survival rates in patients with TNBC and non-TNBC who received neoadjuvant chemotherapy. TNBC, triple-negative breast cancer; CI, confidence interval.

A total of 7 studies (10,15–17,24,25,30) reported the 5-year OS rate in patients with TNBC or non-TNBC who received NAC. There was no heterogeneity between the results of the different studies (I2=5%, P=0.39), so the fixed-effects model was applied for data analysis. The 5-year OS rate in the patients with TNBC was significantly lower than that in the patients with non-TNBC (62.5 vs. 80.7%; OR, 0.52; 95% CI, 0.42–0.65; Fig. 4).

Figure 4.

Figure 4.

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Forest plot: 5-year overall survival rates in patients with TNBC and non-TNBC who received neoadjuvant chemotherapy. TNBC, triple-negative breast cancer; CI, confidence interval.

Survival rate of patients with TNBC as a function of pCR

For the 7 studies (10,16,22,27,28,30,31) that reported the 5-year DFS rate in the patients with TNBC who received NAC according to the achievement of a pCR, there was no heterogeneity between the results (I2=0%, P=0.49), therefore, the fixed-effects model was applied for data analysis. The 5-year DFS rate was significantly higher among the patients with TNBC who achieved a pCR than among those who did not achieve a pCR (OR, 7.42; 95% CI, 4.09–13.48; Fig. 5).

Figure 5.

Figure 5.

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Forest plot: 5-year disease-free survival rates in patients with triple-negative breast cancer who received neoadjuvant chemotherapy according to the achievement of a pCR. CI, confidence interval; pCR, pathological complete response.

For the 7 studies (10,16,21,22,27,30,31) that reported the 5-year OS rate in patients with TNBC who received NAC according to the achievement of a pCR, there was also no heterogeneity between the results (I2=0%, P=0.59), therefore, the fixed-effects model was applied for data analysis. The 5-year OS rate was significantly higher among the patients with TNBC who achieved a pCR than among those who did not achieve a pCR (OR, 6.74; 95% CI, 3.63–12.52; Fig. 6).

Figure 6.

Figure 6.

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Forest plot: 5-year overall survival rates in patients with triple-negative breast cancer who received neoadjuvant chemotherapy according to the achievement of a pCR. CI, confidence interval; pCR, pathological complete response.

Association between molecular marker expression and pCR in patients with TNBC following NAC

A total of 6 studies (12,18,20,23,26,28) reported the association between molecular marker expression and the pCR rate in the patients with TNBC who received NAC. A pooled study of 4 of these studies (12,20,23,26) showed that the patients with TNBC and high Ki-67 expression achieved significantly higher pCR rates than those with low Ki-67 expression (OR, 9.87; 95% CI, 3.53–27.62; Fig. 7). In addition, two pooled analyses of p53 (18,26,28) and CK5/6 (12,20,26) levels revealed no association between these molecules and pCR rate (P>0.05; Figs. 8 and 9).

Figure 7.

Figure 7.

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Forest plot: Pathological complete response as a function of the Ki-67 expression level in patients with triple-negative breast cancer who received neoadjuvant chemotherapy. CI, confidence interval.

Figure 8.

Figure 8.

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Forest plot: Pathological complete response as a function of the p53 expression level in patients with triple-negative breast cancer who received neoadjuvant chemotherapy. CI, confidence interval.

Figure 9.

Figure 9.

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Forest plot: Pathological complete response as a function of the CK5/6 expression level in patients with triple-negative breast cancer who received neoadjuvant chemotherapy. CK, cytokeratin; CI, confidence interval.

Quality evaluation

The quality of the meta-analysis was evaluated using the GRADE framework and is shown in Table II. The quality of the investigation of the 5-year DFS rate in the patients with TNBC with or without a pCR was high. The quality for the study of the 5-year DFS rate in the patients with TNBC or non-TNBC was low. The other assessments were considered to be of moderate quality. The main reason for the lower quality was publication bias. For example, in Fig. 10, the lower left region of the funnel plot is vacant, with points distributed throughout the remainder of funnel, suggesting a publication bias; this may be due to the difficulty in publishing studies with negative results. In Fig. 11, the points in the inverted funnel plot show homogeneous distribution on each side, suggesting no clear publication bias.

Table II.

Grading of Recommendations Assessment, Development and Evaluation framework assessment of eligible studies.

Design Quality assessment No. of eligible studies Quality
Outcome Experiment Control Publication bias Inconsistency Indirectness Imprecision
pCR TNBC Non-TNBC Yes No No No 14 Moderate
5-year DFS TNBC Non-TNBC Yes No No Yes   6 Low
5-year OS TNBC Non-TNBC No No No Yes   7 Moderate
5-year DFS pCR Non-pCR No No No No   7 High
5-year OS pCR Non-pCR Yes No No No   7 Moderate
pCR High Ki-67 Low Ki-67 Yes No No No   6 Moderate
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TNBC, triple-negative breast cancer; DFS, disease-free survival; OS, overall survival; pCR, pathological complete response.

Figure 10.

Figure 10.

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Funnel plot: Pathological complete response in patients with TNBC and non-TNBC who received neoadjuvant chemotherapy. TNBC, triple-negative breast cancer; OR, odds ratio; SE, standard error.

Figure 11.

Figure 11.

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Inverse funnel plot: 5-year disease-free survival rates in patients with triple-negative breast cancer who received neoadjuvant chemotherapy according to the achievement of a pathological complete response. OR, odds ratio; SE, standard error.

Discussion

Patients with TNBC generally have aggressive cancer with higher metastatic and lower survival rates than those with non-TNBC. However, TNBC patients generally achieve a higher pCR rate following NAC treatment compared with those individuals with other subtypes of breast cancer, as was confirmed by the present meta-analysis. In the current meta-analysis, the 5-year DFS and OS rates of patients with TNBC who received NAC were lower than those of patients with non-TNBC. However, a significant improvement in the 5-year DFS and OS rates was apparent in the patients with TNBC who achieved pCR as a result of NAC treatment, suggesting that NAC significantly improves the survival of patients with TNBC, but only for those who show a pCR to treatment.

Certain studies have suggested that different NAC regimens have a different effect on the pCR in breast cancer patients. For example, patients achieve a higher pCR rate and long-term survival rate when paclitaxel is used in anthracycline-based NAC regimens (8,32). In addition, platinum-based NAC regimens also affect the survival rate (33). The NAC regimens of eligible studies in the present meta-analysis were mostly anthracycline and/or paclitaxel regimens.

TNBC can be classified as chemosensitive or chemoresistant (34), distinguished by an analysis of the tumoral expression of molecular marker genes, including EGFR, CK5/6, cyclooxygenase-2, Y-box binding protein-1, B-cell lymphoma 2, Ki-67 antigen and p53 tumor suppressor. It is generally easier to achieve a pCR in patients with chemosensitive disease, therefore, an analysis of molecular marker expression in patients with TNBC would be useful in predicting the response to NAC. The current meta-analysis showed that patients with TNBC characterized by high levels of Ki-67 antigen expression achieved a higher pCR rate than those with low-level expression, suggesting that Ki-67 could be used as a predictor of prognosis and for the selection of patients who would derive the greatest clinical benefit from NAC. However, more studies are required to confirm the association between Ki-67 and patient prognosis. A clinical trial has reported that patients with TNBC can benefit from chemotherapy combined with molecularly targeted therapy in the form of poly-ADP ribose polymerase inhibition, and more detailed studies are underway (35).

The TNM stages of the patients included in the present meta-analysis were I-III/II-III. Therefore, it is possible that the ambiguity of the cancer stage could have introduced a bias in the data; however, the quality of these studies was considered to be mostly moderate on analysis. In addition, the overall results were reliable despite a certain degree of publication bias.

In summary, despite moderate quality and a certain degree of publication bias, a number of conclusions can be made. The survival rates in the patients with TNBC were significantly lower than those in patients with non-TNBC, but the patients with TNBC achieved a higher pCR rate in response to NAC treatment. Furthermore, the patients with TNBC who achieved a higher pCR rate in response to NAC treatment showed significant improvement in survival rates. Finally, high Ki-67 expression was positively correlated with a higher pCR rate, whereas p53 and CK5/6 expression did not display any prognostic function. Future multicenter randomized controlled trials would provide additional support to the current study and aid in determining whether other molecular markers can act as prognostic factors.

Acknowledgements

This meta-analysis was supported by the Programme for National Natural Science Foundation of China (grant no. 30800278) and the Doctoral Fund of Ministry of Education of China (Youth Scholars; grant no. 200804861048).

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