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Clinical Observations |
1 Department of Diagnostic Radiology, Research Institute of Radiological
Science, Yonsei University College of Medicine, Seodaemun-ku Shinchon-dong
134, Seoul 120-752, South Korea.
2 Department of Surgery, Yonsei University College of Medicine, Seoul, South
Korea.
Received January 16, 2007;
accepted after revision July 3, 2007.
Address correspondence to E. K. Kim
(ekkim{at}yuhs.ac).
Abstract
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CONCLUSION. Additional contralateral breast cancers in bilateral synchronous breast cancers are apt to be small and less palpable and to have less suspicious imaging findings and less advanced cancer staging than the index cancer. Bilateral whole-breast sonography with mammography is useful in the early detection of contralateral synchronous breast cancer.
Keywords: bilateral breast cancer • breast cancer • mammography • synchronous cancer • sonography
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The purpose of this study was to compare the clinical, radiologic, and pathologic findings of index and contralateral cancers of bilateral synchronous breast cancers and to retrospectively determine the role of mammography and bilateral whole-breast sonography in the detection of contralateral cancers.
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Study Population
The medical records of all patients who underwent surgery for primary
breast cancer at our institution during the period 2000 through 2006 were
retrospectively reviewed. Between September 2000 and July 2006, 2,465 cases of
stages 0-III primary breast carcinomas, as defined by the American Joint
Committee for Cancer (AJCC)
[10], were treated by either
mastectomy or breast conservation therapy at the department of general surgery
at our institution. Of those 2,465 cancers in 2,419 patients, 72 cancers in 36
patients were classified as bilateral synchronous breast cancer. The lesions
were considered synchronous if they were diagnosed within 6 months. Ten
cancers in five patients, for which preoperative mammography or sonography was
not available, were excluded, and the remaining 62 cancers in 31 patients made
up the material for the comparison of imaging findings. These 31 patients had
undergone both mammography and bilateral whole-breast sonography in their
preoperative evaluations. The contralateral synchronous cancers were detected
at a clinical examination or preoperative imaging evaluation.
Imaging Evaluation
Mammography was performed with dedicated equipment (DMR, GE Healthcare)
until April 2005, and with the Selenia Full-Field Digital Mammography System
(Lorad/Hologic) from May 2005 until the present. Standard craniocaudal and
mediolateral oblique views were routinely obtained, and additional
mammographic views were obtained as needed. Bilateral whole-breast sonography
has been prospectively performed in the preoperative evaluation of a patient
with a known breast malignancy or in the diagnostic evaluation of a patient
with a suspicion of breast cancer in our institution since 2000. Sonography
was performed using ATL HDI 5000 and 3000 (Philips Medical Systems) sonography
units with 10-MHz of linear array transducers by two full-time board-certified
radiologists having 4 and 10 years of experience in performing breast
sonography and in interpreting both breast sonography and mammography. One of
the two radiologists reviewed the record of the imaging studies to gather
category classification, and the other radiologist reviewed imaging
findings.
The BI-RADS categories of mammographic and sonographic findings [11] were used in category classification of the original radiology reports. The original reports were not reread to rule out the possibility that foreknowledge of the correct cancer diagnosis might affect reinterpretation and to ensure that the results would reflect the accuracy of routine diagnostic work. Although the sonography BI-RADS lexicon did not exist before 2003, sonographic findings at our institution had been categorized according to the risk of malignancy similar to mammographic BI-RADS categories since 1999. Before 2003, we had subclassified category 4 into categories 4a and 4b, and regarded category 4b as category 4c of the published sonography BI-RADS lexicons with respect to the risk of malignancy. Since 2003, we have subclassified category 4 into categories 4a, 4b, and 4c. However, category 4b classified after 2003 was preserved as category 4b. Mammographic findings were classified as either mass, mass with microcalcifications, microcalcifications only, focal asymmetry, and architectural distortion, if any abnormality was detected. The sonographic findings were classified according to lexicon of the American College of Radiology BI-RADS [11].
Data Analysis
We defined the index cancer as the mass that was initially detected or
reported by a patient, and contralateral cancer was defined as the mass that
was detected in the contralateral breast during breast evaluation. When the
patient complained of palpable bilateral masses, we regarded the mass that was
palpated first as the index breast cancer. If both the bilateral masses were
asymptomatic, we defined the earlier reported mass as the index breast cancer.
We evaluated clinical and pathologic findings in index and contralateral
cancers; assessed the detection method of all bilateral synchronous breast
cancer cases; and compared the clinical, mammographic, sonographic, and
pathologic findings with each other. For the size of the breast cancer, we
evaluated the invasive cancer only, excluding in situ lesions. The
sensitivities of mammography and sonography were compared.
Statistical comparisons were performed using the Mantel-Haenszel chi-square test for pathologic staging and BI-RADS categorization, the chisquare or Fisher's exact tests for other nonparametric variables, and the Student's t-test for parametric inference. Statistical analysis was performed with the SAS system (MAGREE SAS Macro program).
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The contralateral cancers were more often nonpalpable (84%) than the index cancers (16%), and the difference was statistically significant (p < 0.0001) (Table 1). The contralateral cancers significantly included more cases of ductal carcinoma in situ (DCIS) (45.2%) than the index cancers (9.7%; p = 0.01) (Tables 1 and 2).
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The mean pathologic size of all invasive cancers was 2.2 cm (range, 0.2-12.0 cm; median, 1.7 cm). The contralateral cancers were smaller (mean size, 1.5 cm; median, 1.2 cm; SD, 0.7 cm) than the index cancers (mean size, 2.6 cm; median, 2.4 cm; SD, 2.2 cm; p = 0.04). Seven percent of the index cancers were 1.0 cm or less in diameter compared with 40% of the contralateral cancers (p = 0.02). Table 2 summarizes the distribution of histologic subtypes of the bilateral breast cancers. In the two patients with invasive lobular carcinoma as the index cancer, the contralateral cancers were also invasive lobular carcinoma.
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Among 14 cases of contralateral DCIS, four, including one palpable lesion, showed positive results at both mammography and sonography. Although two DCIS showing microcalcifications were detected on mammography only, and the remaining eight (57%) were found on sonography only, all manifested as masses. Of four DCIS showing positive results on both mammography and sonography, three manifested only as microcalcifications in a dense breast on mammography but revealed combined masses on sonography.
Imaging Findings
Table 4 summarizes the
imaging findings and BI-RADS categorization in 62 bilateral breast cancers.
The index and contralateral cancers showed statistically significant
differences in the mammographic presentation (p = 0.007, Fig.
1A,
1B,
1C), BI-RADS final assessment
(p < 0.001), sonographic boundary (p = 0.038), and
posterior echogenicity (p = 0.005), but no significant differences in
other sonographic findings, including shape (p = 0.210), margin
(p = 0.155), orientation (p = 0.522), internal echogenicity
(p = 0.330), and calcifications (p = 0.306). No
statistically significant differences were noted in mammographic parenchymal
pattern (p = 1.0) because all of our patients except one had
heterogeneously dense or extremely dense breasts and the bilateral mammograms
were performed simultaneously.
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In this study, contralateral cancers tended to be smaller and to have DCIS in a higher percentage of the cases than the index cancer, which is consistent with previous reports. A large portion of index cancers in our patients were detected by palpation (81%, 25/31 patients). This high percentage is unusual in this era of screening, although Hungness et al. [6] also reported 81% of index cancers in their bilateral synchronous breast cancers were diagnosed by palpation (30/37 cases). In a review of the literature, we could not find any other reports about the mode of detection of the index cancer. One of the possible reasons for this high palpability rate in our study is that mammographic screening has just become common in recent years in our country. Second, breast parenchyma in our mammographic examinations showed dense parenchymal tissue in all but one patient. Our patients were approximately 10 years younger than those in previous studies [3, 8, 14, 15], so their mammographic sensitivity might be lower. The third is ethnic differences. Because breast size in Asian American women is reported to be significantly smaller than that in white women [16], we suggest that the small breast volume of the Asian women who were included in our study would reflect a higher rate of palpability. Despite the high rate of palpability, the index cancers in our study were pathologically less than stage 1 in 41.9% (13/31) of patients, which is comparable to the 49.4% in the study by Heron et al. [3] (n = 47), and 68% of palpable index cancers (17/25 patients) were DCIS or stage 1 cancer.
In several previous reports of patients with bilateral breast cancer, the contralateral cancer was small and frequently detected on mammography [6-8]. Murphy et al. [17] reported that bilateral breast cancers frequently showed a similar mammographic appearance to the index cancer and mirror image locations, whereas Roubidoux et al. [14] reported that the contralateral tumors usually have major mammographic findings different from those of the first cancers, and that evaluation of a contralateral mammogram should be performed without regard for the mammographic findings of the first cancer. Our results showed that the most common major mammographic finding was mass with or without microcalcifications in the index cancer, whereas negative mammographic findings were the most common finding in the contralateral cancer. These results are in keeping with those by Roubidoux et al. in that the mammographic signs of the first cancer do not indicate the most likely appearance of cancer in the contralateral breast. As we mentioned, our data are derived from low mammographic sensitivity because of dense parenchymal tissue and the small size of the contralateral breast cancer. However, our results do not diminish the important role of mammography because two of our contralateral cancers manifested microcalcifications on mammograms but showed negative findings on sonograms. Mammography is undoubtedly the cornerstone of breast evaluation.
Saarela et al. [15] compared the results of mammography and sonography for unilateral and bilateral breast cancer; however, they reported 60% sensitivity for sonography in the detection of breast cancer but they did not evaluate the sonography findings. Because standardized terminology such as BI-RADS lexicon did not exist when Saarela et al. reported their work, it was difficult to compare the sonography findings between the unilateral and contralateral breast cancers. We suggest that our results constitute the first report on sonographic findings of bilateral breast cancer and that the appearance of contralateral synchronous breast cancer does not differ from that of the index cancer except for the posterior echogenicity and boundary. However, the final BI-RADS assessment of the contralateral cancer tended to show less suspicious findings than that of the index cancer (p < 0.001), probably because of the smaller tumor size, the smaller amount of posterior shadowing, and fewer palpation findings.
Our results also suggest that sonography of contralateral breasts in patients with breast cancer needs to be approached with more caution than in patients without known breast cancer, and that we should search for any subtle suspicious findings during sonography in these patients. Moon et al. [9] reported that bilateral whole-breast sonography could depict mammographically and clinically unsuspected cancers in the contralateral and ipsilateral breasts. Their result of 12.5% of additional malignant foci found only on bilateral whole-breast sonography supports our results. Our retrospective review of the bilateral synchronous breast cancers that underwent bilateral whole-breast sonography confirmed that sonography had an important role in detecting the contralateral breast cancer.
One of our contralateral cancers was detected on breast MRI, and second-look sonography showed a microlobulated nodule corresponding to the lesion identified on MRI. MRI of the breast shows great promise as a preoperative planning procedure for defining the extent of cancer in the breast and detecting contralateral breast cancer; bilateral whole-breast sonography can be time-consuming and operator-dependent. Berg et al. [18] reported that the combination of MRI, mammography, and clinical examination in the identification of tumor foci was better that any other combinations of tests.
Several reports have indicated that the rate of mammographically and clinically occult contralateral cancers detected on MRI ranged from 3.1% to 11% [19-23]; moreover, some contralateral cancers included sonographically occult cancers [20, 22]. Thus, MRI may be more sensitive in identifying the second, contralateral cancer than sonography and mammography. However, MRI presents some practical limitations: difficulty in interpretation and sampling of lesions depicted only on MRI for biopsy, and the simultaneous evaluation of the contralateral breast requiring technical support such as parallel imaging for bilateral high-resolution MRI [24, 25]. Otherwise, the evaluation of the contralateral breast needs two patient visits and two contrast injections for bilateral sagittal imaging. In our patients, 61.5% of contralateral cancers detected on sonography only were DCIS. The sensitivity of MRI for detecting DCIS is 40-100% [26], so we were not sure that all of the in situ cancers detected only on sonography in our study would be found on MRI.
Patients with bilateral synchronous breast cancer have lower survival rates because of distant metastases, but these results are based on data from one to four decades ago [3, 4, 7, 8, 12]. Although the detection of bilateral synchronous breast cancer on mammography has also been reported to be associated with earlier stage at diagnosis and better survival [7, 8], our study, which was supported by high-resolution sonography, had far fewer palpable bilateral synchronous breast cancers (19%) and much more in situ bilateral synchronous breast cancer (45%) than previous studies (25-35%, 22-26%, respectively) of the early detection of bilateral synchronous breast cancer with mammography [7, 8]. In addition, to prove the survival benefit of bilateral whole-breast sonography, reevaluation of the survival rate in patients with bilateral synchronous breast cancer using sonography-detected contralateral cancer will be needed.
Our study has some limitations. First, the size of our series was too small to make a conclusive inference. Second, our study was done as a retrospective review, so we could not assess the positive predictive value and false-positive biopsy rate of bilateral whole-breast sonography. Further prospective analysis of a larger population to determine the sensitivity, specificity, and positive predictive value for call-backs, for additional imaging, and for biopsy recommendations will be required to evaluate and compare the true accuracy of each detection method. Third, all of our study population consisted of Asian women. Because the breast size in Asian American women is reported to be significantly smaller than that in white women [16], bilateral whole-breast sonography may be easier to perform in Asian women. That our study population consists of all Asian women could affect our results and act as a selection bias. Therefore, further study should be performed with various ethnic groups to generalize our results to other populations.
In conclusion, additional contralateral breast cancers in bilateral synchronous breast cancers tend to be small and less palpable and to manifest as less suspicious imaging findings with a less advanced cancer stage. Our study suggests that bilateral whole-breast sonography with mammography contributes to the early detection of the contralateral cancer of bilateral synchronous breast cancer.
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