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Original Research |
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 General Surgery, Yonsei University College of Medicine, Seoul,
South Korea.
3 Department of Oncology, Yonsei University College of Medicine, Seoul, South
Korea.
Received June 8, 2007;
accepted after revision September 4, 2007.
Address correspondence to E. K. Kim.
Abstract
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MATERIALS AND METHODS. We retrospectively reviewed the pathologic, mammographic, and sonographic records of 51 patients with surgically proven metachronous bilateral breast cancer in 2,498 surgically proven breast cancers during 2000–2006. We first evaluated cancer staging according to the method of detection used to identify metachronous breast cancers. The sensitivity of imaging studies to identify the lesions was also assessed. We compared cancer staging on the basis of whether the patient was included in a screened group, which was one in which a mammogram and sonogram were obtained within 12 months of the pathologic diagnosis of metachronous cancer. Within the screened group, we compared cancer staging on the basis of whether a screening sonogram was obtained within 6 months of the diagnosis of metachronous cancer.
RESULTS. The staging of metachronous cancers showed no statistically significant differences related to detection method. The sensitivity of sonography was 94% and of mammography was 80% in the detection of metachronous cancers. The cancer stage in the screened group was 0 or stage I in 81% and that in the unscreened group was stage II or III in 71% (p < 0.05). Among the screened group, no significant difference was seen in staging regardless of whether a screening sonogram was obtained in the 6 months after diagnosis of metachronous cancer (p = 0.576).
CONCLUSION. Sonography alone detected 14% of metachronous contralateral breast cancers. The results of this study suggest that annual additional sonography with mammography contributes to the early detection of metachronous cancers. However, sonography every 6 months is unlikely to be helpful for the early detection of metachronous cancer.
Keywords: breast cancer • breast cancer screening • breast sonography • women's imaging
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This study retrospectively assessed the role of sonographic surveillance in the early detection of metachronous contralateral breast cancer.
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Study Population
The medical records of all patients who underwent surgery for primary
breast cancer in our institution from February 2000 to November 2006 were
retrospectively reviewed. During that time, 2,498 patients with American Joint
Committee on Cancer (AJCC) [9]
stage 0–III primary breast carcinoma were treated by either mastectomy
or breast conservation therapy by general surgeons at our institution. Among
them, 60 patients had undergone surgery for a contralateral breast malignancy
after definite treatment of an opposite-breast carcinoma. Excluded from the
study were patients with a lobular carcinoma in situ or a borderline phyllodes
tumor as the sole histopathologic finding in the prior primary breast lesions
(n = 3) and patients who underwent an operation for breast cancer
within 6 months of an operation for contralateral cancers (n = 4),
which were defined as synchronous cancers. Of the remaining 53 patients with
metachronous contralateral breast cancers, the medical records or imaging
findings were not available for two patients and both were excluded. Finally,
we included 51 patients with metachronous contralateral breast cancers in our
study population. These 51 patients had undergone both mammography and
bilateral whole-breast sonography in the preoperative evaluations. They had
also undergone both whole-body bone scanning and chest CT to rule out
metastasis in their preoperative evaluations. None of the patients included in
this study had distant metastases.
Surveillance and Retrospective Imaging Evaluation
All patients with breast cancer had undergone preoperative mammography and
bilateral whole-breast sonography at our institution since 2000
[10]. Clinical follow-up
examinations after breast cancer surgery were performed every 6 months for the
first two or three postoperative years and then annually thereafter. During
the follow-up examinations, patients with invasive breast cancers were advised
to undergo annual mammography and bilateral whole-breast sonography every 6
months for the first 2 years and annual mammographic and sonographic
evaluations thereafter. The patients with ductal carcinoma in situ (DCIS) were
advised to undergo annual mammographic and sonographic evaluations. In
patients who had undergone a mastectomy for breast cancer, sonographic
evaluations of the chest wall and contralateral breast were performed. The
interval of imaging studies was somewhat variable because of patient
preference and examination scheduling. Some of our patients could not or did
not accept our recommended protocol because of their schedules.
Mammograms were obtained with dedicated equipment before April 2005, and a full-field digital mammography system (Selenia Full Field Digital Mammography System, Lorad/Hologic) was used beginning in May 2005. 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 our institution since 2000. Each sonogram was obtained using a sonography unit (ATL HDI 5000 or 3000, Philips Medical Systems) with either a 5- to 10-MHz or a 5- to 12-MHz linear-array transducer by one of two full-time board-certified radiologists. The two radiologists had 4 and 10 years' experience, respectively, in performing breast sonography and interpreting breast sonography and mammography at the time of the study. The number of screening breast sonography examinations that each performed in their practice varied from 250 to 350 examinations per month.
Sonographic examinations were performed with patients in the supine position with the arms raised. When necessary, patients were shifted into an appropriate anterior oblique position so that the lateral parts of the breast could be scanned. Scanning was targeted first to the ipsilateral breast or chest wall and then to the contralateral breast during each examination and was performed in radial and antiradial planes, the longitudinal and transverse planes, or both [11]. The examination took approximately 15 minutes (range, 5–25 minutes).
Data Analysis
We evaluated clinical and pathologic findings in metachronous cancers and
assessed the detection method of all cases. We also assessed the detection
method according to the parenchymal pattern on mammograms. Cancer staging was
compared according to the method used to detect metachronous breast
cancers.
Patients were also grouped according to whether a screening mammogram and sonogram had been obtained within 12 months of the pathologic diagnosis of the metachronous cancers. These groups were compared for detection methods and tumor stage. Moreover, the patients who underwent screening mammography and sonography within 12 months of diagnosis of their metachronous cancer were subgrouped as to whether a screening sonogram had been obtained within 6 months of the diagnosis of cancer. These groups were also compared for tumor stage. For the determination of breast cancer size, we evaluated invasive cancer only, excluding in situ lesions. The sensitivity of mammography and the sensitivity of sonography were compared in these cases.
Statistical comparisons were performed using the chi-square or Fisher's exact test for other nonparametric variables and the Student's t test for parametric inference. Statistical significance was assigned to p values less than 0.05. All statistical computations were performed using software (SAS system for Windows, version 9.0, SAS Institute).
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Detection Methods and Their Sensitivity
All of the patients in this study underwent both mammography and
sonography. The methods for detection of metachronous breast cancers are
summarized in Table 1. Overall,
mammography results were true-positive in 41 (80%) of 51 patients, whereas
sonography results were true-positive in 48 (94%) of 51 patients. This
difference, however, was not statistically significant (p = 0.49).
According to the parenchymal pattern of mammography, 14 patients showed
scattered fibroglandular tissues and all of them had metachronous breast
cancer detected by mammography. The remaining 37 patients showed
heterogeneously or extremely dense breast tissue. Ten (27%) of the 37 patients
had metachronous breast cancer for which mammography results were negative
(p = 0.045, Table
1).
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The pathologic stages are compared with the method for detection of the cancers in Table 2. Both of the two metachronous breast cancers detected by mammography alone were DCIS. In the seven metachronous breast cancers detected by sonography alone, five cancers (71%) were stage I or in situ. The remaining two cancers both had metastasis in a single axillary lymph node among approximately 30 dissected lymph nodes, in which the tumor was 1.3 and 2.0 cm, respectively.
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Of the 51 metachronous breast cancers, 26 were detected in the screened group and 17 were not; information about screening mammograms and sonograms obtained before the detection of the other eight breast cancers was inadequate. The pathologic stages of the cancers in the screened group compared with those of the unscreened group are summarized in Table 3. Patients in the screened group were more likely to have DCIS alone (p < 0.007) and less likely to have stage II or III cancers (p < 0.002) than those in the unscreened group. In the screened group, patients who had undergone sonography within the 6 months before the metachronous breast cancer was detected were compared with those who had not (Table 4). This difference in staging, however, was not statistically significant (p = 0.576).
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As others have observed in previous reports [6], we found that cancers in patients who have been screened are smaller and less advanced than those in unscreened patients. Thus, the key points in the surveillance of patients with an operative history of breast cancer are which technique to use for screening and how often screening should be performed. In several previous reports of patients with bilateral breast cancer, the contralateral cancer was small and frequently detected on mammography [6]. In the current study, although all 14 patients who showed scattered fibroglandular tissues had metachronous breast cancers detected by mammography, mammography showed an 80% sensitivity in all the cases and 73% sensitivity in patients with dense breasts, whereas sonography had 94% sensitivity in all the cases. These results were derived from low mammographic sensitivity due to the small size of breast cancers in dense parenchymal tissues.
Our results suggest that sonography screening is more helpful for women with dense breast tissue. However, our results do not diminish the important role of mammography because two of our metachronous cancers manifested microcalcifications on mammograms but showed negative findings on sonograms. Mammography is undoubtedly the cornerstone of breast evaluations.
The necessity of bilateral whole-breast sonography in the preoperative evaluation of patients with breast cancers has been reported [7, 10], and mammography with bilateral whole-breast sonography, MRI, or both as adjunctive tools have been reported to contribute to early detection of contralateral cancer or bilateral synchronous breast cancer [7, 15–18]. Recently, the results of MRI studies about the detection of contralateral cancer were reported [19, 20]: MRI detected cancers in contralateral breasts that were overlooked by clinical examinations, mammography [19], and sonography [20] at the time of initial breast cancer diagnosis in 3.1–18.6% of patients. The mean interval from detection of the first cancer to detection of the second cancer in our study was 82 months, which seemed to be a sufficient period for developing new contralateral cancer, even though breast MRI examinations were performed in our patients at the time of the initial breast cancer diagnosis. Clearly, there could be value in an adjunctive study to mammography, especially in patients with dense breasts, to increase cancer detection and for surveillance. However, for surveillance purposes, no standardized programs have been implemented with respect to these adjuncts until recently, even though follow-up examinations of patients with breast cancer is an integral part of the treatment in most breast oncology centers [21].
Overall, an estimated 30 of every 1,000 (3%) high-risk women screened using MRI will have otherwise occult cancers detected [22]. This is approximately 10 times the yield of mammography in average-risk women. However, this added cancer detection comes at a cost: Current data suggest that the risk of a high-risk woman having abnormal findings on a screening MRI examination that require biopsy is approximately 7–18%, and the positive predictive value of biopsy ranges from 18% to 64%. However, the use of MRI for screening is limited by its high cost, relative lack of availability, variable patient tolerance, and requirement for contrast injection. The criteria for follow-up and risk of malignancy in lesions followed have not been well established. Just as the sensitivity of mammography can be limited because of the degree of high density in surrounding tissue, the sensitivity of MRI depends on the degree of background enhancement. Breast sonography could be a candidate to complement the limitations of MRI.
Saarela et al. [18] compared the results of mammography and sonography for unilateral and bilateral breast cancer and reported a 60% sensitivity for sonography in the detection of breast cancer, whereas the sensitivity of breast sonography in our study was up to 94%. There are several possible reasons for this discrepancy in the findings of these two studies. First, breast sonography is operator-dependent, especially for small lesions [23]. The two radiologists who performed breast sonography in our study had 4 or 10 years' experience performing bilateral whole-breast sonography. The number of screening breast sonography examinations performed by each radiologist in their own practice varied from 3,000 to 4,200 examinations per year. Another possible explanation for the discrepant findings is the sonography equipment used. Saarela and colleagues used a 5- or 7.5-MHz linear transducer, but a linear-array transducer greater than 7 MHz is recommended for breast sonography [24, 25]. Another explanation may be ethnic differences. Because the breast size of Asian American women is reported to be significantly smaller than that of white women [26], we suggest that the smaller breast volume of Asian women included in our study is suitable for breast sonography. The difference for sensitivity is further explained by the fact that breast sonography in the study by Saarela et al. [18] did not target the whole breast but, rather, the palpable or mammographically detected area. A total of 59% of our cases (30 of 51 metachronous cancers) were nonpalpable and 23% of those (seven of 30 cancers) were detected by sonography alone. All of the cancers detected by sonography alone were DCIS or stage T1, which suggests that sonography has an important role in the detection of contralateral metachronous breast cancers and synchronous breast cancers and that sonography could be an adjunctive tool in addition to mammography in the surveillance of breast cancer patients.
Rosselli Del Turco et al. [27] and the investigators of the Italian Interdisciplinary Group for Cancer Evaluation (GIVIO) [28] reported that no significant differences were noted in overall mortality and survival between a group of breast cancer patients who underwent intensive surveillance and a group who underwent routine screening; however, their studies did not include sonography in the screening process. Our study found no differences in staging between patients who had undergone intensive sonography within 6 months of primary breast cancer diagnosis and patients who had undergone sonography 6 months after diagnosis. This result suggests that intensive sonographic evaluation every 6 months contributes little to the early detection of metachronous contralateral breast cancer.
Our study has some limitations. First, the size of our series was small and the follow-up period was short. We could not assess the survival benefit with sonography surveillance, so we could not generalize our retrospective results for sonography surveillance and intensive sonography surveillance until its efficacy has been proven scientifically. Future prospective studies with a larger population should be performed. Second, we did not assess the frequency of further study rates or false-positive biopsy rates arising from adjunctive sonography. With any study looking at the usage of a technique for screening, it is only fair that some analyses reveal the number of false-positives. To accept breast sonography as a screening technique, a prospective study with a larger population would be required. These additional evaluations would increase the cost for surveillance because sonography screening is not covered by many health care providers. More research should be performed to determine whether sonography surveillance is cost-effective and beneficial to the survival rate.
In conclusion, 14% of the metachronous breast cancers evaluated in our study were detected by sonography alone. Our results suggest that annual sonography with mammography contributes to the early detection of metachronous cancers, especially in patients with dense breasts on mammography, whereas intensive sonography every 6 months contributes little to the early detection of contralateral cancers.
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