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Year : 2015  |  Volume : 11  |  Issue : 5  |  Page : 89-94

Clinicopathological features of invasive lobular carcinoma of the breast: A nationwide multicenter study in China

1 Department of Breast Surgery, Zhejiang Cancer Hospital, Banshanqiao, Hangzhou, China
2 Department of Cancer Epidemiology, Center of Breast Disease, Beijing; Department of Pathology, Cancer Institute and Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China
3 Depatment of Breast-Thyroid Surgery, Xiangya Second Hospital, Central South University, Changsha, China

Date of Web Publication31-Aug-2015

Correspondence Address:
Prof. H J Yang
Department of Breast Surgery, Zhejiang Cancer Hospital, No. 38, Guangji Road, Banshanqiao, Gongshu District, Hangzhou 310000
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0973-1482.163851

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 > Abstract 

Objective: To analyze the clinicopathological features of invasive lobular carcinoma (ILC) and compare them with invasive ductal carcinoma (IDC), hoping to find the fact of ILC in China and assist the decision makers with proper individualized treatment.
Materials and Methods: A nationwide multicenter retrospective study was performed. A total of 4211 primary breast cancer cases were randomly selected from 1999 to 2008 in seven regions of China. ILC cases were compared with IDC by clinicopathological features and molecular subtypes.
Results: A total of 135 (3.2%) ILC and 3471 (82.4%) IDC cases were included for analysis. The age, tumor size, menopausal state, family history, nodal status, and stage of ILC were similar to that of IDC. ILC was more likely to be positive for estrogen receptor (65.5% vs. 57.7%) and progesterone receptor (64.7% vs. 58.5%), and less likely to overexpress human epidermal growth factor receptor-2 (17.3% vs. 23.6%). Even though, these differences are not significant, the proportion of luminal A type of ILC is significantly larger than that of IDC (54.8% vs. 42.7%; P < 0.05).
Conclusion: ILC has a larger proportion of luminal A type compared with IDC. Larger sample size study for better known of molecular subtypes of ILC is needed in future to individualize the treatment decision.

Keywords: Epidemiologic study, human epidermal growth factor receptor-2, lobular neoplasm, molecular subtype, steroid receptor

How to cite this article:
Zhu M Z, Yu X F, He X M, Feng W L, Fan J H, Li J, Xu F, Tang Z H, Zhang B N, Qiao Y L, Zheng S, Yang H J. Clinicopathological features of invasive lobular carcinoma of the breast: A nationwide multicenter study in China. J Can Res Ther 2015;11, Suppl S1:89-94

How to cite this URL:
Zhu M Z, Yu X F, He X M, Feng W L, Fan J H, Li J, Xu F, Tang Z H, Zhang B N, Qiao Y L, Zheng S, Yang H J. Clinicopathological features of invasive lobular carcinoma of the breast: A nationwide multicenter study in China. J Can Res Ther [serial online] 2015 [cited 2023 Jan 27];11, Suppl S1:89-94. Available from: https://www.cancerjournal.net/text.asp?2015/11/5/89/163851

 > Introduction Top

Invasive breast cancer is the most common cancer and the leading cause of cancer death in women from many countries around the world. [1],[2] In China, according to the most updated data of cancer registration in 2009, the incidence rates were 23.16/100,000 and 28.99/100,000, respectively after standardized by the age structure of China and the world. Besides, the age-standardized rates of mortality were 4.94/100,000 and 6.56/100,000. [2]

First described as a distinct histologic type of breast cancer by Foote and Stewart in 1946, [3] invasive lobular carcinoma (ILC) is the second most common histological type of breast malignancy after invasive ductal carcinoma (IDC) and constitutes about 5-15% of all breast cancers. [4] Earlier studies have suggested that the prevalence of ILC increased steadily due to the use of combined hormone replacement therapy over the period from 1987 to 1999 while the incidence rates of IDC remained essentially constant. [5],[6],[7] In contrast, the incidence rate of ILC decreased from 1999 to 2004 related to a reduced use of combined hormone replacement therapy. Furthermore, this decline was much greater than that of IDC. [8] The distinct difference in the change of incidence in ILC and IDC may suggest that ILC is more sensitive to the effects of hormone therapy than IDC.

As a distinct entity, ILC differs from IDC in several clinicopathological features and the reaction to systemic therapy. The classic, or pure, ILC shows cells in single file, producing finger-like strands and characterized by the E-cadherin loss. [4] ILC is frequently associated with older age and has more favorable parameters with high levels of expression of the hormonal receptor, no overexpression of human epidermal growth factor receptor-2 (HER-2) and in general of low-grade. [9],[10] Clinically, ILC often fails to form discrete, palpable masses. However, a subtle diffuse area of thickening or skin retraction may be the only clinical abnormality, and this make the clinical diagnosis challenging. [3],[11] ILC may spread via lymphatic or hematogeneous dissemination. ILC is less likely to affect the lungs, pleura, and central nervous system compared with IDC. In contrast, ILC is more likely to involve the bones, peritoneum, ovary, and gastrointestinal system. [9],[12] It is thought that the loss of adhesiveness due to the loss of expression of the cell-cell adhesion molecule E-cadherin in ILC facilitates the difficulty of detective and the form of metastases. [9] Katz et al. reviewed a large quantity of randomized trials of neoadjuvant chemotherapy and noted that ILC has a substantially lower rate of pathological complete response to neoadjuvant chemotherapy than IDC. However, the long-term outlook seems better. [13] This enhanced situation might have been the result of sensitivity to endocrine therapy after completion of systemic chemotherapy and surgery.

Although the unique clinicopathological features of ILC, the treatment options currently are the same with IDC. We conducted this nationwide multicenter retrospective study in China to explore the ILC trend over a period of 10 years and compare the clinicopathological features of ILC with IDC, in the hope of providing scientific data for decision makers with proper treatment of this special entity.

 > Patients and Methods Top

Patient selection

China was stratified into seven geographic regions (North, North-East, Central, South, East, North-West, and South-West). One of the best leading hospitals from each region was selected. From 1999 to 2008, 45,200 patients with breast cancer were treated in the seven hospitals [Figure 1]. We identified the study group by random sampling of this population. In each hospital, 1-month was randomly selected to represent each year from 1999 to 2008. January and February were excluded for randomization because the traditional Chinese spring festival is always in these 2 months, and there are much fewer inpatients during the time period. To avoid selection bias, an enrollment scheme was adopted by using alternating prespecified months of inpatient admission from year to year. For example, in the 1 st year (1999) of data collection, patients with pathology-confirmed primary breast cancer admitted to inpatient treatment in March would be enrolled in the study; in the 2 nd year (2000), inpatients admitted in April would be enrolled. All inpatient cases within the selected month were reviewed, and their information was collected. In months with fewer than 50 cases, the cases from the previous and following months were reviewed until a total of 50 were reached. When there were more than 50 cases in the selected month, all cases in that month were reviewed. All patients met the following inclusion criteria: (1) Pathologically confirmed primary breast cancer, (2) inpatient admission date within the selected month in the study hospital, and (3) treatment (surgery, chemotherapy, or radiotherapy) for breast cancer was recorded. The detailed randomization methods and the basic characteristics of the patients can be referred in these published studies. [14],[15]
Figure 1: Geographic distribution of seven hospitals in the study. (1) North; Beijing (2) North-East; Liaoning (3) Central; Hunan (4) South; Guangdong (5) East; Zhejiang (6) North-West; Xi'an (7) South-West; Sichuan

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Data collection

A total of 4211 primary breast cancer patients from the randomly selected months were analyzed. The clinical data, histological findings, and tumor, node, metastasis (TNM) stages of all patients were reviewed. The histological diagnose was based on the WHO classification of tumors of the breast. [4] Estrogen receptor (ER) and progesterone receptor (PR) were measured by immunohistochemical staining and regarded as positive when more than 1% was stained. Tumors were considered HER-2 + if the FISH test was positive or if the HercepTest-score was 3+ (>30% of the cells with mutation) and HER-2 if the HercepTest-score was 0 (<10% of the cells expressed the mutation). In case of HercepTest-score 2 (10-30% of the cells expressing the mutation), the FISH test was performed. Breast cancer subtypes are classified by St. Gallen molecular subtype classification in 2011: Luminal A (ER + and/or PR + , Ki67 low and HER-2 ), luminal B (ER + and/or PR + , Ki67 high and/or HER-2 + ), HER-2 + (ER , PR and HER-2 + ) and triple-negative (ER , PR , HER-2 ). [16] We classified breast cancer subtypes by ER, PR and HER-2 in our study because the data of Ki67 was not available.

Statistical analysis

SPSS statistical software version 17.0 (Pfizer Inc., New York) was used to analyze the data. The Chi-square test was used to compare the difference between ILC and IDC by clinicopathological features. The difference was considered as significant if the P < 0.05.

 > Results Top

A total of 4211 primary breast cancer cases were identified. 135 (3.2%) ILC and 3471 (82.4%) IDC cases were picked out for detailed analysis of clinicopathological features. In our study, all cases of ILC were pure. Representative pathological features for ILC and IDC are presented in [Figure 2]. The percentage of ILC in the total number of breast cancer every year during that period ranges from 0.2% to 4.2% [Table 1].
Figure 2: Immunohistological distinction of invasive lobular carcinoma and invasive ductal carcinoma by E-cadherin. The lobular carcinoma cells loosely cohesive with each other (a: H and E, ×100; b: H and E, ×200). E-cadherin is not detected on the cell membrane (c). In contrast, ductal carcinoma cells display rather cohesive arrangement (d: H and E, ×100; e: H and E, ×200), and E-cadherin is distinctively expressed on the cell membrane (f)

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Table 1: The number of ILC and IDC cases by year

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The average age was 48.0 years (standard deviation [SD] = 9.6 years) and 48.7 years (SD = 10.3 years) in the patients with ILC and IDC, respectively. The average tumor size was 30.5mm (SD = 17.1 mm) and 30.8 mm (S.D. =16.5 mm) in ILC and IDC, respectively. Compared with IDC, menopausal state, family history and TNM stage were similar to that of IDC. ILC was more likely to be positive for ER (65.5% vs. 57.7%) and PR (64.7% vs. 58.5%), and less likely to overexpress HER-2 (17.3% vs. 23.6%), but no statistical significant difference was observed. However, the proportion of luminal A type of ILC is significantly larger than that of IDC (54.8% vs. 42.7%; P < 0.05). The clinical and pathologic characteristics of ILC compared with IDC are summarized in [Table 2], [Table 3], [Table 4].
Table 2: Comparison of clinicopathological characteristics between ILC and IDC of the breast (part 1)

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Table 3: Comparison of clinicopathological characteristics between ILC and IDC of the breast (part 2)

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Table 4: Comparison of clinicopathological characteristics between ILC and IDC of the breast (part 3)

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 > Discussion Top

This nationwide multicenter retrospective study is the first geographically representative epidemiologic study of breast cancer across the entire country. By means of collecting this data, we can have a thorough view of the actual situation regarding ILC in China.

An obvious increasing or decreasing trend of ILC is absent during this 10 years period. Percentage of total ILC in the total invasive breast cancer observed in the present study (3.2%) is lower compared with reported literature (5-15%). [4] The explanation for this discrepancy mainly is, all cases of ILC enrolled in our study are pure ILC, while other variant subtypes of ILC and ILC-IDC mixed type were excluded.

It has been reported that ILC occurs more among older women than IDC, with the median age at diagnosis being around 56 years. [17],[18],[19] In this study, the median age of ILC was 48.0 years, similarly with the median age of IDC (48.7 years). The discrepancy of our result compared with reported data drew our attention that the age of breast cancer in China is probably much younger, and the majority of them are premenopausal. This was similar to the findings from other regional studies within China. [20],[21],[22],[23],[24],[25] However, larger sample size study is needed for detailed analysis of the age of ILC in China. On the other hand, the relation of age to local recurrence in some reports suggested that ILC patients aged 45 years or younger had a significantly higher risk of local recurrence after 5 years of follow-up. [26] In this study, we did not collect the follow-up data and could not analyze the prognosis of the younger sample.

ILC does not always have obvious clinical features as a result of infiltrative growth pattern and multifocal development, resulting in the challenge to be detected. [9] ILC often presents with subtle mammographic features, such as asymmetric densities and architectural distortions. The sensitivity of mammography for detecting ILC has been reported to range between 57% and 79%, whereas the false-negative rates are up to 19%. [27],[28],[29] The ultrasound appearance of ILC usually likes a heterogeneous, hypoechoic mass with ill-defined margins and a posterior acoustic shadow. However, the sensitivity of ultrasound for the detection of ILC is greater than that of mammography. [30] Magnetic resonance imaging is extremely sensitive for the detection of ILC and maybe more precise to evaluate the extent of the disease, agreeing well with pathological examination. [31],[32] Due to the lack of discrete mass formation and difficulty in diagnosis, the tumor size observed in ILC is reported to be larger than other types of invasive breast cancer. [33],[34] In the present study, the mean tumor size of ILC was similar to the size of IDC in the pathological examination. Furthermore, the proportions of T categories were similar between ILC and IDC. Consequently, the feature of relative larger tumor size of ILC in our study was not observed. And this may draw our attention for further study.

Lymph node metastasis of ILC is considered to be more frequent than IDC. [10] However, the N categories of ILC were similar to IDC in this study. The M categories were not significantly different between them, either. We had better do further analysis of the N status by different T categories to explore the susceptible feature of lymph node metastasis of ILC. Nevertheless, we were regretful to find that we failed to collect the data by different T categories.

The high rate of ER and PR positivity and low rate of HER-2 overexpression in ILC presented in our study, although there's no statistically significant, is consistent with previous studies. [9],[10] Breast cancer has been identified several intrinsic subtypes that can predict distinct clinical outcomes. These subtypes were originally identified by gene expression analysis using DNA microarrays, which were based on an intrinsic gene list of 496 genes that differentiate breast cancers into separate groups through different gene expression patterns. [35] The intrinsic subtypes include two main subtypes of ER tumors (basal-like and HER-2 + /ER subtype) and ER + tumors (luminal A and luminal B). [36] However, large-scale subtyping using gene expression profiling from formalin-fixed, paraffin-embedded samples individually is not currently feasible. In 2011, the St. Gallen International Breast Cancer Conference suggested a surrogate definition of intrinsic subtypes of breast cancer by combining biological markers. [35],[37] The luminal A subtype (ER + and/or PR + , Ki67 low and HER-2 ) has the best favorable prognosis and systemic treatment is restricted to endocrine therapy. The luminal B subtype (ER + and/or PR + , Ki67 high and/or HER-2 + ) has a high proliferation rate and/or a high histological grade and chemotherapy followed by endocrine therapy is recommended. [38] The HER-2 + subtype (ER , PR and HER-2 + ) appears particularly prone to early and frequent relapse, recommended for treatment with the anti-HER-2 monoclonal antibody trastuzumab. [39] The triple negative subtype (ER , PR , HER-2 ) has been associated with poor clinical outcomes, which is likely due to the lack of directed therapies since ER and HER-2 . [40] A significantly larger proportion of luminal A type of ILC was observed in our study. This may indicate that ILC is biologically different from IDC. As a result, endocrine therapy should be strongly considered in ILC, and the outcome will be better compared with IDC.

 > Conclusion Top

This is the first nationwide study on ILC that compared biologic characteristics with IDC. Our study reflects the fact of ILC in China. The data shows clearly that ILC and IDC are distinct entities with different clinical and pathologic phenotypes. We tentatively put forward that ILC has a larger proportion of luminal A type as a result of favorable characteristics such as more likely to be positive for ER/PR and less likely to overexpress HER-2. Larger sample size and the age of ILC in China should be further studied. More detailed analysis of pathologic features such as Ki67 is also needed in the further study. Besides, the systemic therapy like endocrine therapy and chemotherapy, as well as the follow-up of ILC, should be learned to precisely predict the outcomes across breast cancer subtypes. A better known of the differences of breast cancer subtypes is required to direct and individualize treatment decisions in future.


We thank the Cancer Institute of the Chinese Academy of Medical Sciences for providing their expertise in the development of this study. We also thank the local investigators from Beijing, Liaoning (Shenyang), Hunan (Changsha), Guangdong (Guangzhou), Zhejiang (Hangzhou), Shannxi (Xian), and Sichuan (Chengdu) for data collection and assisting us with completing this project successfully. The authors thank Pfizer for funding.

Financial support and sponsorship

The study was supported by a grant from Pfizer.

Conflicts of interest

There are no conflicts of interest.

 > References Top

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  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3], [Table 4]

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