Clinicopathological Characteristics of Mucinous Breast Cancer: a Retrospective Analysis of a 6-year Study From National Cancer Center in Vietnam

doi:10.21203/rs.3.rs-4951346/v1

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Clinicopathological Characteristics of Mucinous Breast Cancer: a Retrospective Analysis of a 6-year Study From National Cancer Center in Vietnam

https://doi.org/10.21203/rs.3.rs-4951346/v1

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published 23 Oct, 2024

Read the published version in Breast Cancer Research and Treatment →

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Purpose: To evaluate clinicopathological features in women with mucinous breast cancer (MBC), distinguishing between pure (PMC) and mixed (MMC) subtype.

Methods: A retrospective analysis of all 358 women with MBC treated at Vietnam National Cancer hospital from June 2015 to December 2020. PMC was defined by ≥ 90% mucinous components.

Results: We identified 358 women with MBC (245 PMC and 113 MMC) representing 2.7% of all 13,254 BC patients. The proportion of stage I, II, III and IV were 34.9%, 50.8%, 10.4% and 3.9% respectively. The rate of HER2 overexpression is 12%, in which only 1.4% of patients was treated with anti-HER2. 193 patients (53.9%) had chemotherapy, including 55 patients (15.4%) treated in neoadjuvant setting. Only 3 patients (5.5%) achieved pCR.

PMC patients were older (54.4±13.3 vs 51.1±13.1 years), had lower Ki67 expression, lower incidence of nodal metastasis (N+) (p values <0.05). At median follow-up of 58 months, the 5-year overall survival rate of non-metastatic patients was 86.6%. Multivariate analysis showed N+ to be the most significant prognostic factor (HR=3.3; 95%CI 1.5-7.1), followed by T (HR=2.9; 95%CI 1.4-6.3), HER2+ (HR=2.5; 95%CI 1.2-5.3) and MMC subtype (HR=1.9; 95%CI 1.0-3.9). Amongs 245 patients with stage T1-2N0M0, 40.8% of those treated with CT related to worse overall survival (5-year OS 88.0% vs 95.6%, p=0.04)

Conclusion: Poor prognostic factors of MBC include high T, N stage, HER2 overexpression and MMC subtype. CT in stage T1-2N0M0 brings worse survival outcome. Given the low response rate to neoadjuvant CT, upfront surgery is appropriate for MBC patients.

Mucinous breast cancer (MBC)

Pure mucinous carcinoma (PMC)

Mixed mucinous carcinoma (MMC)

Chemotherapy (CT)

Breast cancer is one of the most common cancers in women with increasing number of cases and the leading cause of death[1]. Mucinous breast carcinoma (MBC) is a uncommon type, representing about1–6% of all invasive breast cancers[2]. MBCs are associated with more favorable prognosis compared to invasive ductal carcinoma (IDC)[3]. MBC is categorized into two main subtypes: pure mucinous carcinoma (PMC) and mixed mucinous carcinoma (MMC)[4]. PMC is characterized by the dominance of mucinous components, accounting for ≥ 90% of the tumor composition, whereas MMC comprises less than 90% mucin alongside other architectural patterns such as lobular or ductal breast cancer[5]. PMC typically correlates with a more promising prognosis, associated with younger age, smaller tumor size, and less frequent nodal involvement[6].

MBC tends to be associated with older age, with the median age at diagnosis being 71 years, compared to 61 years in patients with IDC[7]. MBCs typically exhibit positivity for estrogen and/or progesterone receptors (ER/PR-positive), alongside low expression of androgen receptors (AR), and negativity for human epidermal growth factor receptor 2 (HER-2)[8]. Furthermore, MBCs demonstrate a lower incidence of axillary lymph node (ALN) metastasis and distant metastasis compared to other types of breast cancer, such as ductal or lobular carcinoma[9, 10]. The rate of metastatic disease and regional nodal involvement were about 2% and 12% for PMC respectively.

Clear recommendations for the clinical management of mucinous breast carcinoma (MBC) remain elusive. 2013 St. Gallen consensus conference for the first time described a separate treatment strategy for MBCs as endocrine-responsive type[11]. Subsequently, the 2014 National Comprehensive Cancer Network (NCCN) guidelines acknowledged MBC as a favorable subtype. Present guidelines suggest that for hormone receptor-positive tumors without nodal involvement, adjuvant endocrine therapy (ET) may be deferred if tumor size is less than 1 cm. However, consideration of ET is warranted for tumors sized between 1 and 3 cm, while it is strongly recommended for tumors larger than 3 cm. Chemotherapy is considered if patients have nodal involvement. Although prior studies indicate a significant portion of MBC patients receive adjuvant chemotherapy, its efficacy in improving survival remains uncertain, while its use may lead to side effects and toxicity[12],[13]. Given the good prognosis of MBC, adjuvant chemotherapy may be an overtreatment. Nonetheless, the existing literature on outcomes and treatments primarily derives from small-scale studies with limited follow-up periods, leaving treatment guidelines for MBC ambiguous. Therefore, this study aimed to evaluate clinicopathological features and prognosis in women with mucinous breast cancer (MBC), distinguishing between pure (PMC) and mixed (MMC) subtype and determine the rate of adjuvant chemotherapy and its benefits in different subgroups of MBCs.

Study design

The study is a retrospective analysis of all 358 women with MBC treated at Vietnam National Cancer hospital from June 2015 to December 2020. PMC was defined by ≥ 90% mucinous components. This study was approved by the Ethical Committee of the Vietnam National Cancer Hospital.

Eligible participants and Materials

We included patients with a pathological diagnosis of MBC from June 2015 to December 2020, according to the WHO Classification of Tumors of the Breast 2012.

The clinicopathological data were collected from medical records and pathology reports, including age at diagnosis, TNM stage, histologic grade, number of metastatic lymph nodes (LNs), lymph vascular invasion (LVI), expression of estrogen receptor (ER), progesterone receptor (PR), and human epidermal growth factor receptor-2 (HER2), as well as the type of adjuvant treatment. If the tumor was defined as MMC, immunohistochemistry (IHC) was performed on a non-mucinous part. HER2 positive were defined as 3 + by IHC or 2 + on IHC and positive by fluorescence in situ hybridization (FISH), while IHC 0/1 + or FISH- were considered HER2 negative. TNM classification was designated according to the 8th edition of the American Joint Committee on Cancer.

Statistical analysis

The data were analyzed using SPSS Statistics for Windows, version 26.0 (IBM Corp., Armonk, USA). Continuous variables were presented as medians and ranges, while categorical variables were expressed as percentages. For continuous variables, the Student's T-test was applied, and for categorical variables, either the Chi-square test or Fisher's exact test was used.

Survival analysis included overall survival (OS) for all MBC, PMC, and MMC subtypes, as well as an assessment of the survival benefit of adjuvant chemotherapy for MBC. OS was defined as the time from the initial breast cancer diagnosis to death from any cause. The Kaplan-Meier method and log-rank test were employed to evaluate survival differences. Univariate and multivariate analyses for OS utilized a Cox proportional hazard ratio (HR) model. A p-value < 0.05 was considered statistically significant.

Patient characteristics

Table 1

Clinicopathological characteristics of Pure Mucinous Carcinoma (PMC) and Mixed Mucinous Carcinoma (MMC) treated in Vietnam National Cancer hospital from June 2015 to December 2020.
Characteristics No. (%)	PMC (n = 245)	MMC (n = 113)	Overall (n = 358)	p value
Metastasis, No. (%) No Yes	234 (95.5) 11 (4.5)	110 (97.3) 3 (2.7)	344 (96.1) 14 (3.9).9)	0.31
Age, years, No. (%) ≤ 50 > 50	112 (45.7) 133 (54.3)	64 (56.6) 49 (43.4)	176 (49.2) 182 (50.8)	0.03*
Ki67 status, No. (%) ≤ 20 > 20 Unknown	161 (65.7) 55 (13.5) 29 (11.8)	58 (57.4) 43 (42.6) 12 (10.6)	219 (61.2) 98 (27.4) 41 (14.4)	0.002*
ER status, No. (%) Negative Positive Unknown	8 (3.3) 226 (92.2) 11 (4.5)	7 (6.2) 100 (88.5) 6 (5.3)	15 (4.2) 326 (91.1) 17 (4.7)	0.25
PR status, No. (%) Negative Positive Unknow	42 (17.1) 192 (78.4) 11 (4.5)	24 (21.2) 83 (73.5) 6 (5.3)	63 (19.9) 253 (80.1) 17 (4.7)	0.22
Her2 status, No. (%) Her2 negative Her2 positive Unknow	187 (76.3) 27 (11.0) 31 (12.7)	86 (76.1) 16 (14.2) 11 (9.7)	273 (76.3) 43 (12.0) 42 (11.7)	0.59

A total of 358 women with MBC (245 PMC and 113 MMC) with available medical records were enrolled in this study, representing 2.7% of all 13,254 breast cancer patients. 49.2% of patients were than 50 years of age. The proportion of stage I, II, III and IV were 34.9%, 50.8%, 10.4% and 3.9% respectively; 326 (91.1%) and 273 (76.3%) patients were ER-positive and HER-2 negative, respectively. Only 2.8% of patients had triple negative breast cancer (TNBC). The rate of HER2 overexpression is 12%, in which only 1.4% of patients were treated with anti-HER2 therapy. PMC patients were older (54.4 ± 13.3 vs 51.1 ± 13.1 years), and had lower Ki67 expression.

Table 2

Clinicopathological characteristics of non-metastasis pure mucinous carcinoma (PMC) and mixed mucinous carcinoma (MMC) treated in Vietnam National Cancer hospital from June 2015 to December 2020.
Characteristics Non-metastasis No. (%)	PMC (n = 234)	MMC (n = 110)	Overall (n = 344)	p value
T stage, No. (%) ≤ 20 mm > 20 mm	110 (47.0) 124 (53.0)	56 (50.9) 54 (49.1)	166 (48.4) 178 (51.6)	0.3
N status, No. (%) Negative Positive	190 (81.2) 44 (18.8)	65 (59.1) 45 (40.9)	254 (74.1) 89 (25.9)	< 0.001*
Chemotherapy, No. (%) No Yes	135 (57.7) 99 (42.3)	30 (27.3) 80 (72.7)	165 (48.0) 179 (52.0)	< 0.001*
Chemotherapy type, No. (%) Adjuvant Neodjuvant	71 (71.7) 28 (28.3)	53 (66.2) 27 (33.8)	124 (69.3) 55 (30.7)	0.26
Response, No. (%) pCR PR SD PD	2 (7.1) 13 (46.4) 11 (39.3) 2 (7.1)	1 (3.7) 15 (37.0) 10 (55.6) 1 (3.7)	3 (5.5) 28 (50.8) 21 (38.2) 3 (5.5)	0.21

Among non-metastatic patients, PMC patients had lower incidence of nodal metastasis (N+) than MMC patients (p value < 0.001). There was no difference in tumor size between the two groups (p-value = 0.3). The rate of chemotherapy (CT) was 53.9%. Fifty-five patients (15.4%) were treated in neoadjuvant setting (28 PMC and 27 MMC). Among those who received neoadjuvant CT, only 3 patients (5.5%) achieved pCR. Meanwhile, the rates of PR, SD and PD were 50.8%, 38.2% and 5.5% respectively. In terms of adjuvant chemotherapy, a higher proportion of MMC patients received adjuvant chemotherapy compared to PMC ones (72.7% versus 42.3%, p < 0.001).

Prognostic factors in MBC and efficacy of chemotherapy for MBC

Median follow-up was 58 months. The 5-year overall survival rate was 86.6%. Univariate analysis revealed that significant factors for poorer OS were MMC subtype (p = 0.02), large tumor size (T) (p < 0.001), nodal metastasis N+ (p < 0.001), HER2 positive (HER2+) (p < 0.001), PR negative (p = 0.02), metastasis (p < 0.001) and high Ki67 (p = 0.02). Meanwhile, multivariate analysis showed N + to be the most significant prognostic factor (HR = 3.3; 95%CI 1.5–7.1), followed by T (HR = 2.9; 95%CI 1.4–6.3), HER2+ (HR = 2.5; 95%CI 1.2–5.3) and MMC subtype (HR = 1.9; 95%CI 1.0-3.9). Chemotherapy in multivariate analysis did not significantly improve the survival prognosis (HR = 1.2; 95%CI 0.5–2.9). Moreover, among 245 patients with stage T1-2N0M0, 40.8% of those treated with CT related to worse overall survival (5-year OS 88.0% vs 95.6%, p = 0.04)

Mucinous breast carcinoma (MBC) is an uncommon type of well-differentiated invasive adenocarcinoma, characterized by the production of varying amounts of extracellular epithelial mucus. At our institution, the incidence of mucinous breast carcinoma (MBC) was 2.7% (358 out of 13,254 cases), falling within the commonly reported range of 1–6% in the literature. The majority of patients (96%) presented at stage I or II, while the proportions for stage III and IV were 10.4% and 3.9% respectively. This result is consistent with published data, supported the hypothesis that MBC displays a less aggressive behavior[14].

These tumors also showed a high proportion of hormone receptor expression, with 91.1% being positive for estrogen receptors and 80.1% for progesterone receptors in our study. According to Komenaka et al., ER and PR were positive in 91% and 79% of MBC[14]. The high hormone receptor expression rate indicated a favorable prognosis. The rate of HER2 overexpression of MBC in Vietnam was higher than previous studies, and there is non-significant difference in the rate of Her2 overexpression between PMC and MMC. Typical MBC IHC express positivity for estrogen receptor (ER) and progesterone receptor (PR), but negativity for HER2[7]. While HER2 overexpression accounted for about 15–20% of invasive breast cancers[15], many previous studies reported that that rate was only 2.6–9.0% in MBC[7]. According to Jang, 4.8% of PMC showed HER2 positivity[16]. Some studies showed that the incidence of HER2 overexpression in MBC was 5.8–9.5%[17]. In our study, HER2 positivity is higher at 12% and was significantly associated with poor OS in univariate and multivariate analyses[16]. While HER2-targeted therapy is essential treatment for these patients, the rate of HER2 overexpression patients who received anti-HER2 therapy in our study was only 1.4%. This contributed to the worsening outcome of patients with HER2-positive MBC.

MBC can be categorized into pure (PMC) and mixed (MMC) based on the assessment of mucinous component[18]. PMC is characterized by the exclusive presence of tumor tissues with mucinous components comprising more than 90%, whereas MMC includes mucinous areas covering more than 50% but less than 90% of the total area typically mixed with infiltrating ductal epithelial components[19]. Differentiating between the two types of carcinomas is crucial due to the significantly better prognosis associated with pure mucinous carcinoma compared to the mixed type. Mucus production in mucinous breast cancer is suggested a good prognostic factor, as mucin potentially acts as a mechanical barrier, diminishing tumor cell invasion at the margins and leading to less aggressive tumor biology[20]. Previous publishes have shown the differences in clinicopathological features and survival between PMC and MMC[21]. Our analysis demonstrated that patients with PMC were older (54.4 ± 13.3 vs 51.1 ± 13.1 years) and had lower Ki67 expression than patients with MMC. Consistent with published data, MMC has a greater rate for lymph node metastasis compared to PMC. Previous studies show that axillary nodal positivity in PMC ranges from 0–29%, compared to 17–65% in MMC[21]. It has been suggested that lymph node metastases are more likely to arise from the invasive ductal component. Adjuvant therapy was more frequently given to patients with MMC (72.7% of MMC patients compared to only 42.3% of PMC patients). Despite the favorable prognosis of MBC, many clinicians used adjuvant chemotherapy similar to that used for other types of breast cancer[22],[23]. The rate of chemotherapy in our study is even higher than previous study, up to 52.0%[24]. Clinical experience with neoadjuvant therapy for mucinous carcinoma is limited. According to Haiying, only 2 out of 28 (7%) mucinous carcinomas demonstrated a complete pathologic response[25]. In our study, this proportion was 5.5% (3 out of 55). According to a case report by Baretta et al., even MBC with subtype of HER-2 positive that exhibits resistance to neoadjuvant chemotherapy with trastuzumab[26]. The low response rate seen in mucinous carcinoma treated with neoadjuvant chemotherapy is likely because the mucin acted as a barrier against chemotherapy. Moreover, despite chemotherapy effectively eliminating malignant cells, these mucin pools tend to persist.

We found a 86.6% 5-year survival rate in MC patients which is a lower 5-year OS rate compared to other clinical studies. When considering subgroups, we identified a superior overall survival (OS) in PMC patients compared to MMC patients (p-value = 0.02). Many previous studies have shown that the presence of metastasis in axillary lymph nodes is the strongest predictor of survival due to the potential of distant metastasis[27]. In our study, ALN metastasis was also the most significant prognostic factor for OS, while MMC subtype (p = 0.02), large tumor size (T) (p < 0.001), HER2 positivity (p < 0.001), PR negativity (p = 0.02), metastasis (p < 0.001) and high Ki67 (p = 0.02) were significant prognostic factors for OS. Our findings on multivariate analysis showed that adjuvant chemotherapy did not significantly improve OS in most MBC patients. Furthermore, among 245 patients with stage T1-2N0M0, 40.8% of those treated with CT related to worse overall survival (5-year OS 88.0% vs 95.6%, p = 0.04).

Our study had several potential limitations. Due to the retrospective design and limitations in data assessment, a significant portion of data was missing, particularly pathological details and treatment information.

In conclusion, the results of this large retrospective analysis revealed that poor prognostic factors of women with MBC include high T, N stage, HER2 overexpression and MMC subtype. CT in stage T1-2N0M0 brings worse survival outcome compared to endocrine therapy. Given the low response rate to neoadjuvant CT, upfront surgery is appropriate for MBC patients.

Mucinous breast cancer (MBC), Pure mucinous carcinoma (PMC), Mixed mucinous carcinoma (MMC), Chemotherapy (CT)

ACKNOWLEDGMENTS

We thank our collages at Vietnam National Cancer Hospital for their valuable help in the study.

STATEMENTS & DECLARATIONS

The authors declare that they have no conflicts of interest or financial ties to disclose with the contents of this article.

FUNDING

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

COMPETING INTERESTS

The authors have no relevant financial or non-financial interests to disclose.

AUTHOR CONTRIBUTIONS

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Thi Hoai Hoang and Thanh Long Nguyen. The first draft of the manuscript was written by Thi Hoai Hoang and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

DATA AVAILABILITY

The datasets generated during and/or analysed during the current study are not publicly available but are available from the corresponding author on reasonable request.

ETHICS APPROVAL

This is an observational study. The Vietnam National Cancer Hospital Research Ethics Committee has confirmed that no ethical approval is required.

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You are reading this latest preprint version

Clinicopathological Characteristics of Mucinous Breast Cancer: a Retrospective Analysis of a 6-year Study From National Cancer Center in Vietnam

Status:

Journal Publication

Version 1

Abstract

Figures

INTRODUCTION

MATERIALS AND METHOD

Study design

Eligible participants and Materials

Statistical analysis

RESULTS

Patient characteristics

Prognostic factors in MBC and efficacy of chemotherapy for MBC

DISCUSSION

ABBREVIATIONS

Declarations

References

Additional Declarations

Status:

Journal Publication

Version 1