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10.1245/ASO.2003.01.007
Annals of Surgical Oncology 10:740-747 (2003)
© 2003 Society of Surgical Oncology
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ORIGINAL ARTICLES

Small Invasive Breast Carcinomas in Taiwanese Women

Tzu-Chieh Chao, MD, PhD, Miin-Fu Chen, MD, Chia-Siu Wang, MD, Yi-Yin Jan, MD, Tsann-Long Hwang, MD and Shin-Cheh Chen, MD

From the Division of General Surgery, Department of Surgery, Chang Gung University College of Medicine; and Chang Gung Memorial Hospital, Taoyuan, Taiwan.

Correspondence: Address correspondence and reprint requests to: Tzu-Chieh Chao, MD, PhD, Department of Surgery, Chang Gung Memorial Hospital at Keelung, 222 Maichin Road, Keelung, Taiwan; Fax: 886-22433-2655; E-mail: tcchao{at}adm.cgmh.org.tw


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Female Taiwanese breast cancer patients are younger than their Western counterparts. This study examined the predictors of axillary lymph node metastases in Taiwanese women with T1 breast cancer.

Methods: Data from 394 Taiwanese women with T1 invasive breast carcinoma were retrospectively reviewed.

Results: The data contained 6 T1a, 51 T1b, and 337 T1c breast tumors. The patients’ ages ranged from 23 to 82 years (mean ± SD, 48.2 ± 11.4 years; median, 46.4 years). Axillary nodal metastases were present in 38.3% of the patients (16.7% in T1a, 35.3% in T1b, and 39.2% in T1c tumors). The patients with nodal metastases had significantly greater body weights and S-phase fractions than those without nodal metastases. Univariate analysis revealed that unfavorable pathology, lymphovascular invasion, S-phase fraction >7%, and nondiploid DNA ploidy were significantly associated with lymph node metastases. Lymphovascular invasion was the only significant variable as the independent predictor in the multiple logistic regression analysis. In the Cox proportional hazards regression analysis, axillary nodal status and lymphovascular invasion were significantly associated with survival.

Conclusions: Taiwanese women with small breast cancer displayed a relatively higher incidence of axillary lymph node metastases than Western women. Axillary lymph node dissection or sentinel lymph node biopsy should be conducted on Taiwanese patients with small invasive breast carcinomas, particularly when risk factors exist.

Key Words: Breast cancer • DNA ploidy • Lymphovascular invasion • Lymph nodes • S-phase fraction • Survival


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The incidence of small breast carcinoma increases with public awareness of the potential benefits of early detection of breast cancer and improvement of imaging modalities. Invasive breast carcinomas measuring <=1 cm represented just 5.4% of all cases identified between 1977 and 1982,1 yet this increased to 29% between 1989 and 1993.2 Axillary lymph node status and tumor size are the two most reliable indicators in the prognosis for breast cancer survival.3–5 The incidence of axillary lymph node metastases associated with invasive breast carcinomas measuring <=2.0 cm (T1) varies from 21% to 32%.6–12 The rate of occurrence of positive lymph nodes in T1a (<=.5 cm) and T1b (>.5 and <=1.0 cm) invasive breast carcinomas was 0% to 11.0% and 10% to 19.4%, respectively.6,10,13,14 On the basis of these findings, some authors have suggested that routine axillary lymph node dissection may be avoided in select groups of patients with small breast carcinoma.2,11,12,14 However, other authors recommend that axillary dissection be a standard approach for all patients with small invasive carcinoma of the breast.15–18

For many years, axillary dissection has been a routine method for determining the status of axillary lymph nodes. However, axillary dissection may cause complications, such as thrombosis of the axillary vein, injury to the motor nerve of the axilla, edema of the arm and breast, seroma formation, and shoulder dysfunction.19 Sentinel lymph node biopsy is an alternative to axillary dissection that has fewer complications. Nevertheless, the success rate of sentinel lymph node biopsy in predicting the presence or absence of nodal metastases varies with patient age, location of the primary carcinoma, and histological examination method and also varies among surgeons.20,21 Therefore, it is necessary to study predictive factors for the status of axillary lymph nodes to avoid unnecessary axillary dissections.

Compared with many Western countries, Taiwan is considered to have a low incidence of breast cancer, with an estimated age-adjusted incidence of 15 to 20 per 100,000, which is much lower than the 60 to 90 per 100,000 in the United Kingdom or the United States.22 Furthermore, breast cancer patients in Taiwan tend to be younger than in Western countries.23 US studies revealed that Asian women with breast cancer were younger than white women and had a better 5-year survival rate.24,25 Although numerous studies of Western women affected by T1 breast cancer have been reported in medical literature,6–12 data on Taiwanese patients with T1 invasive breast carcinoma are generally lacking. Pitfalls have been shown to exist in applying the results of published studies across different populations26,27; thus, this work examined the relationship between clinicopathological factors and axillary lymph node metastases in Taiwanese women with small invasive breast carcinoma.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
During a 4-year period from 1995 to 1998, 469 patients with breast carcinomas measuring <=2 cm (T1) were treated at the Division of General Surgery, Chung Gung Memorial Hospital, Taoyuan, Taiwan. The data from these patients were then retrospectively reviewed. Tumor size was determined on the basis of macroscopic measurement of the tumor and breast ultrasound, and the larger of the two dimensions was used for analysis. These tumors, as classified by the staging system of the American Joint Committee on Cancer,28 include T1a (<=.5 cm), T1b (>.5 and <=1.0 cm), and T1c (>1.0 and <=2.0 cm) breast tumors. The following cases were excluded from the analysis: ductal carcinoma-in-situ, lobular carcinoma-in-situ, noncarcinoma cases, and cases in which no lymph nodes or one to nine lymph nodes were examined. After these exclusions, the study comprised 394 invasive carcinoma cases.

The following tumor characteristics were studied: the presence of lymphovascular invasion, Scarff-Bloom-Richardson (SBR) grade, estrogen receptor status, progesterone receptor status, DNA ploidy, and S-phase fraction. Estrogen and progesterone receptor analysis was conducted with the dextran-coated charcoal method or immunohistochemical staining. Information was not available for all patients because of small tumor size. Patients were grouped according to the following criteria: age (<=40 vs. >40 years), tumor size (<=1.0 vs. >1.0 cm), histological type (favorable vs. unfavorable), SBR nuclear grade (1 vs. 2 and 3), axillary lymph node status (positive vs. negative), estrogen receptor (positive vs. negative), progesterone receptor (positive vs. negative), DNA ploidy (diploid vs. nondiploid), and S-phase fraction (<=7% vs. >7%). Cases with unfavorable histologies were defined as those with invasive ductal carcinoma, infiltrating lobular carcinoma, and medullary carcinoma, whereas cases with favorable histologies included mucinous carcinoma, papillary carcinoma, and tubular carcinoma.

Continuous data were expressed as mean ± SD. The unpaired Student’s t-test was used to compare continuous data within groups. The {chi}2 test was used to compare clinical and pathologic characteristics with respect to nodal status in univariate analyses. Multiple logistic regression analysis was used to determine the independent variables that predict nodal status. Disease-specific survival was defined as the interval between diagnosis and last follow-up. Patients who were alive or had died of a cause other than breast cancer were censored for analysis of disease-specific survival. Disease-specific survival was calculated by the Kaplan-Meier method and was compared by using the log-rank test. The effect of prognostic variables on survival was analyzed with the Cox proportional hazards regression model. P < .05 was considered statistically significant. All analysis was performed with StatView statistics software, version 5.0.1 (SAS Institute Inc., Cary, NC).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Of 394 patients with T1 invasive breast carcinoma (Table 1), 6 (1.5%) had T1a, 51 (12.9%) had T1b, and 337 (85.5%) had T1c tumors. Of these tumors, 193(49. 0%) occurred in the right and 201 (51.0%) in the left breast. The most common histological finding was invasive ductal carcinoma (327 cases; 83.0%), followed by infiltrating lobular carcinoma (27 cases; 6.9%), medullary carcinoma (14 cases; 3.6%), mucinous carcinoma (13 cases; 3.2%), tubular carcinoma (12 cases; 3.1%), and papillary carcinoma (1 case; .3%).


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  		TABLE 1. Patient and tumor characteristics
 
The mean and median age of all patients was 48.2 and 46.4 years (range, 23–82 years), respectively. Eighty-seven percent of the patients were younger than 60 years, and most were aged 40 to 49 years (Fig. 1). The mean and median size of all tumors was 1.51 and 1.50 cm (range, .3 to 2.0 cm), respectively. Various parameters were compared to examine the differences between the tumors measuring <=1 cm and those measuring >1 cm. The tumors measuring <=1 cm had significantly lower S-phase fraction values than did those measuring >1 cm (5.8 ± 7.1 vs. 8.1 ± 8.0, respectively; P = .0386). Age, body weight, height, body mass index, hemoglobin, WBC, platelets, AST, alkaline phosphatase, creatinine, cancer antigen 15.3, and carcinoembryonic antigen did not differ with variation in tumor size. However, the patients with axillary lymph node metastases displayed significantly higher body weights (59.3 ± 8.9 kg vs. 57.1 ± 9.0 kg; P = .0188) and S-phase fraction (9.5% ± 8.3% vs. 6.6% ± 7.3%; P = .0004) than did those without axillary lymph node metastases. Age, height, body mass index, tumor size, hemoglobin, WBC, platelets, AST, alkaline phosphatase, creatinine, cancer antigen 15.3, and carcinoembryonic antigen did not differ significantly between patients with and without nodal metastases. Thirty-four patients referred from other hospitals with histological confirmation of malignancy did not have breast imaging data. Of the remaining 360 patients, 208 were examined by breast ultrasound and mammography, 130 patients by breast ultrasound only, and 22 patients by mammography only. That is, 338 patients were examined by breast ultrasound and 230 patients by mammography. In the patients examined by ultrasound, 36 (10.7%) had negative ultrasound findings, and their breast tumors were detected by mammography. Conversely, ultrasound detected breast tumors in 16 patients (7.0%) in whom mammography failed to demonstrate the lesions.



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  		FIG. 1. Distribution of patients with invasive breast carcinomas associated with axillary nodal status for various age groups.

 
Two hundred eighty-two (71.6%) patients, including 151 patients with lymph node metastases and 131 patients without lymph node metastases, were treated by postoperative adjuvant chemotherapy with either 9 courses of CMF (cyclophosphamide 600 mg/m2, methotrexate 40 mg/m2, and 5-fluorouracil 600 mg/m2) or 6 courses of CEF (cyclophosphamide 500 mg/m2, epirubicin 70 mg/m2, and 5-fluorouracil 500 mg/m2). CMF was administered to 1 (16.7%) T1a patient, 19 (59.4%) T1b patients, and 187 (75.1%) T1c patients. CEF was given to 13 (40.6%) T1b patients and 62 (24.9%) T1c patients. Of 32 T1b patients who received chemotherapy, 18 patients had axillary nodal metastases and 14 patients did not have nodal metastases. Chemotherapy was administered to these 14 T1b patients without nodal metastases on the basis of the presence of lymphovascular invasion and high S-fraction phase.

A total of 151 patients (38.3%) were found to have axillary lymph node metastases. For T1a, T1b, or T1c tumors, positive lymph nodes were identified in 1 (16.7%) of 6, 18 (35.3%) of 51, and 132 (39.2%) of 337 patients, respectively. Meanwhile, axillary lymph node metastases occurred in 33.3% of tumors measuring <=1 cm and 39.2% of those measuring >1 cm (P > .05). Lymph node metastases were identified in 3 (11.5%) of 26 tumors with favorable histologies; this ratio was significantly lower (P < .05) than that for tumors with unfavorable histologies (40.2%). Univariate analysis of categorized tumor characteristics revealed that unfavorable pathology, lymphovascular invasion, greater S-phase fraction, and nondiploid DNA ploidy were the parameters significantly associated with axillary lymph node metastases (Table 2). Tumors without lymphovascular invasion were significantly (P < .05) associated with a lower rate of axillary lymph node metastases compared with those with lymphovascular invasion (32.4% vs. 63.2%). The incidence of lymph node metastases was 33.0% in tumors with S-phase fraction <=7% and was 50.8% in those with S-phase fraction >7% (P < .05). Axillary lymph node metastases occurred in 29.3% of diploid tumors and 49.1% of nondiploid tumors (P < .05). Variables that were statistically significant at the univariate analysis were entered into a multiple logistic regression model, and lymphovascular invasion was the only parameter to remain statistically significant as the independent predictor in the final model (Table 3).


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  		TABLE 2. Univariate analysis of the association between clinicopathologic characteristics and axillary lymph node metastases
 

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  		TABLE 3. Multiple logistic regression analysis of dichotomized tumor descriptors for axillary lymph node metastases
 
There were no survival differences according to age, menopausal status, tumor size, tumor nuclear grade, estrogen receptor status, progesterone receptor status, and chemotherapy. Axillary nodal status, DNA ploidy, S-phase fraction, and lymphovascular invasion were significant variables associated with patient survival (Fig. 2). In the multivariate analysis (Table 4), nodal status and lymphovascular invasion remained significantly associated with survival, although S-phase fraction and DNA ploidy lost their significance.



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  		FIG. 2. Disease-specific survival in patients with invasive breast cancers measuring <=2 cm. SPF, S-phase fraction.

 

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  		TABLE 4. Multivariate proportional hazards regression analysis of survival
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In cases of invasive breast carcinomas, both the frequency and the number of axillary lymph node metastases increase with the number of lymph nodes examined and reach a plateau at 10 examined lymph nodes.29–31 On the basis of these observations, we evaluated a minimum of 10 lymph nodes. This study reports an overall rate of axillary lymph node metastases of 38.3% among 394 Taiwanese women with invasive breast carcinomas measuring <=2 cm. Patients without nodal invasion had a better cumulative survival rate than those with nodal invasion (Fig. 2). Furthermore, univariate analysis revealed that lymphovascular invasion, unfavorable histology, S-phase fraction >7%, and nondiploidy were much more frequently associated with axillary nodal metastases (Table 2). Of these risk factors, multiple logistic regression analysis found lymphovascular invasion to be the only independent predictor of axillary nodal metastases. Similar to our findings, Barth et al.,7 Shoup et al.,10 and Chadha et al.9 have identified lymphovascular invasion as an independent predictor of axillary lymph node metastases in small breast carcinomas. Additionally, Port et al.,15 Abner et al.,8 and Rivadeneira et al.32 also noted that lymphovascular invasion is significantly associated with a higher risk of lymph node metastases. These findings emphasize the importance of this tumor characteristic in forecasting axillary lymph node positivity.

Unlike the findings of Barth et al.7 that S-phase fraction and DNA ploidy could not predict axillary nodal metastases, most authors reported S-phase fraction and DNA ploidy to be accurate indicators of the prognosis for breast cancer patients.9,33–36 Wenger et al.35 demonstrated that S-phase fraction, DNA ploidy, and steroid receptor status were associated with axillary nodal positivity. Ravdin et al.36 found tumor size, patient age, S-phase fraction, and progesterone receptor status to be independent predictors of axillary nodal status in breast cancer patients with tumors of <=5 cm. In addition, the investigation of T1 breast cancer by Chadha et al.9 found S-phase fraction on univariate analysis to be significantly associated with nodal metastases. These findings agree with our findings that S-phase fraction and DNA ploidy are significant predictors of axillary nodal metastases.

Among patients affected by small breast cancer, older patients have a higher incidence of axillary nodal metastases than younger patients.6,9,32 Tumor size is another predictor of lymph node metastases in small breast carcinomas. The incidence of axillary lymph node metastases increases with tumor size; axillary lymph node metastases were present in 0% to 12% of T1a, 10% to 19.4% of T1b, and 24% to 35% of T1c invasive breast carcinomas.2,6–11,14–17,32,37,38 Additionally, nuclear grade is also significantly associated with axillary lymph node metastases.6,7,10,13,32 However, our series demonstrated that patient age, tumor size, and SBR nuclear grade were not significantly associated with axillary lymph node metastases in T1 breast cancer. The discrepancy between our findings and those from other series might be caused by racial differences and different definitions of tumor size. The definition of tumor size in the literature varies significantly, possibly affecting the incidence of positive lymph nodes. Microscopic size may involve the measurement of only the invasive component or may also include the intraductal component. Although it has been suggested that microscopic tumor size is a better predictor of axillary lymph node status than macroscopic size,39 Abner et al.8 demonstrated that the rate of axillary nodal metastases associated with macroscopic tumor size did not differ significantly from that associated with microscopic tumor size. Meanwhile, Yang et al.40 compared tumor size as measured by ultrasound, magnetic resonance imaging, and mammography with pathologic size in 39 patients and concluded that ultrasound is the most valuable imaging method in staging breast cancer. Additionally, some authors have verified that ultrasound can estimate the pathologic size of breast cancer, especially for lesions of <=2 cm.41,42 Consequently, ultrasound-measured tumor size may be used for small breast cancer staging. The larger of the tumor dimensions found by either pathology or ultrasound was used for analysis in this study to avoid bias.

Breast cancer incidence and survival vary with ethnic/racial differences.43,44 Several studies have shown that when Asian women migrate to the United States, the incidence of breast cancer increases in subsequent generations.45,46 Taiwan is considered a low-incidence area for breast cancer as compared with many Western countries.22 In Western countries, the mean age of patients with invasive breast cancer measuring <=2 cm ranges from 58 to 64 years,6,9,10,37 compared with an average age of 48 years in this study, in which 87% of the patients were younger than 50 years. The previously described figures agree with our previous findings for patients with T1 to T3 breast cancer.47 The prognosis for breast cancer has been reported to be good among older women and relatively unfavorable among younger women.48,49 Lyman et al.50 demonstrated that women aged >=65 years had earlier-stage cancer, lower histological grades, higher hormone receptor levels, and lower S-phase fractions than did women <65 years old. Meanwhile, Diab et al.49 reported that in invasive breast cancer patients aged >=55 years, an association existed between increasing age at diagnosis and the tumor’s having more favorable biological characteristics. In their investigation, the rate of axillary nodal involvement in tumors measuring <1 cm was 13% in patients aged 55–64 years and 8% in those >=85 years. Mustafa et al.6 demonstrated that young age is a strong predictor of nodal metastases in both univariate and multivariate analyses of 2185 patients with invasive breast carcinomas measuring <=1 cm. The rate of nodal involvement in patients aged <=40 years was 31.2%, which is in agreement with our findings. Consequently, the relatively young age of our sample may partly explain the high rate of nodal metastases in this series.

Axillary lymph node status is a major determinant of survival in small breast cancers (Fig. 2; Table 4).17,51,52 Routine axillary dissection in patients with small invasive breast cancers remains controversial. In an attempt to avoid the morbidity of axillary dissection, some investigators have advocated sentinel lymph node biopsy or avoidance of dissection in patients with small breast cancers, particularly for T1a tumors.11,38,53,54 They argue that no trial has proven a survival advantage for axillary dissection and that the pathologic characteristics of the primary tumor can provide adequate information for treatment decision making.2,11,12,14,38,54 Nevertheless, other investigators have shown that axillary dissection achieves a better overall survival rate of patients with T1 breast cancer.17,55 They argue that there is a higher incidence of nodal metastases in small breast cancers.1,17,56–58 Besides, the success rate of sentinel lymph node biopsy in predicting nodal metastases varies with patient age, location of the primary carcinoma, and histological examination method and also varies among surgeons.20,21 In patients with T1N0 breast cancer, a significant improvement in disease-free survival occurs in patients with >=10 lymph nodes removed compared with those with <10 lymph nodes removed.18 This observation reflects the potential for the misclassification of tumor stage among patients with fewer nodes removed. Therefore, a complete axillary node dissection is advocated to provide local control and give a good staging procedure to predict patient prognosis.6,51 The finding herein of a 38.3% rate of axillary nodal metastases in patients with small invasive carcinomas suggests that axillary nodal dissection or sentinel lymph node biopsy should be performed for these patients, especially where risk factors exist.

In conclusion, Taiwanese patients with small breast cancers tend to be younger than their Western counterparts. Axillary lymph node metastases and lymphovascular invasion are significant variables associated with survival. Univariate analysis revealed that unfavorable histological types, lymphovascular invasion, S-phase fraction >7%, and nondiploid DNA ploidy are the factors significantly associated with axillary nodal metastases. More than one third of the patients with small invasive breast carcinomas had axillary nodal metastases. Axillary lymph node dissection or sentinel lymph node biopsy should be conducted on Taiwanese patients with small invasive breast carcinomas, particularly where risk factors exist.


   ACKNOWLEDGMENTS
 
The acknowledgments are available online at www.annalssurgicaloncology.org.

The authors thank Dr. Ting-Chang Chang, the director of Biostatistical Consultation Center, Chang Gung Memorial Hospital.


   FOOTNOTES
 
Taiwanese women with T1 breast cancer are younger and display a higher incidence of axillary lymph node metastases than their counterparts in Western countries. Lymphovascular invasion and axillary lymph node metastases were the significant independent variables associated with survival.

Received for publication January 6, 2003. Accepted for publication April 21, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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