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Breast Imaging |
1 From the Departments of Diagnostic Radiology (B.S.E., B.D.F., D.G.B., S.G.P., J.P.) and Pathology (N.S.), University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Box 57, Houston, TX 77030. Received July 10, 2001; revision requested August 20; revision received August 22, 2002; accepted September 26. Address correspondence to B.S.E. (e-mail: bedeiken@di.mdacc.tmc.edu).
| ABSTRACT |
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MATERIALS AND METHODS: Between July 1994 and March 2001, US of the reconstructed breast was performed in 20 women with autogenous myocutaneous flap reconstruction. US findings were correlated with clinical and mammographic findings. US-guided FNAB of 25 (64%) of the 39 recurrent cancers depicted at US was performed.
RESULTS: Twenty-one (54%) of the 39 recurrent cancers depicted at US were clinically occult. Mammography performed in 12 of the 20 patients with reconstructed breasts depicted 14 (56%) of the 25 recurrent cancers that were detected at US in these patients. US-guided FNAB helped to establish a definitive diagnosis of recurrent breast carcinoma in 24 (96%) of the 25 tumor specimens sampled.
CONCLUSION: US and US-guided FNAB are valuable for the assessment of both palpable and clinically occult recurrent breast cancers in autogenous myocutaneous flap breast reconstructions.
© RSNA, 2003
Index terms: Breast, biopsy, 00.1261 Breast, prostheses Breast neoplasms, radiography, 00.11 Breast neoplasms, US, 00.12983, 00.12985, 00.12989
| INTRODUCTION |
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Although routine imaging of the reconstructed breast has not been advocated for the detection of recurrence (6), the results of a study conducted by Slavin et al (7) suggest that the combination of physical examination and mammography is effective in the detection of recurrence. Although the diagnostic accuracies of ultrasonography (US) and US-guided fine-needle aspiration biopsy (FNAB) of breast masses have been established (8,9), to our knowledge, the roles of these procedures in the detection and diagnosis of recurrent breast carcinoma following autogenous myocutaneous flap breast reconstruction have not yet been addressed. Thus, the purpose of our retrospective study was to assess the value of US and US-guided FNAB in the detection and diagnosis of recurrence in breasts reconstructed with autogenous myocutaneous flaps after mastectomy for primary breast cancer, and to describe the US appearances of recurrence in the reconstructed breast.
| MATERIALS AND METHODS |
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At the time of diagnosis of the original breast cancer, the patients ranged in age from 31 to 58 years (mean age ± SD, 46 years ± 8). The histopathologic types of the original tumors in the 20 patients were invasive ductal carcinoma in 13 (65%) patients, ductal carcinoma in situ in four (20%) patients, invasive mixed ductal and lobular carcinoma in two (10%) patients, and medullary carcinoma in one (5%) patient. The clinical tumor stages in 18 patients were known: stage I in seven (39%), stage II in nine (50%), and stage III in two (11%) patients.
The largest diameter of the original breast cancers, which we determined from the mammographic or physical examination reports, ranged from 0.3 to 5.5 cm (mean, 1.9 cm ± 1.6), and one patient had diffuse involvement of the breast. The tumor was solitary in 14 (70%) of the 20 patients, multifocal in five (25%) patients, and involved all quadrants with diffuse microcalcifications without a mass in one (5%) patient.
Treatment for the original cancer included modified radical mastectomy, nodal dissection, and breast reconstruction in all patients (10). In one (5%) of the 20 patients, postoperative radiation therapy (56 Gy) was part of the initial treatment. Ten (50%) of the 20 patients underwent postoperative chemotherapy, and three of these patients had also undergone preoperative chemotherapy.
Breast reconstruction in the 20 patients consisted of free TRAM flaps in 17 (85%) patients, pedicle TRAM flaps in two (10%) patients, and a pedicle latissimus dorsi myocutaneous flap in one (5%) patient (11). Immediate reconstruction following skin-sparing modified radical mastectomy was performed in 19 (95%) patients. In the remaining patient (5%), an implant was placed immediately following mastectomy and free TRAM flap reconstruction was performed 5 months later.
The time between the diagnosis of the primary breast cancer and the diagnosis of recurrence in the reconstructed breast, the initial clinical impression of the palpable abnormality that prompted the request for breast imaging evaluation, the mammographic diagnosis, and the US-based diagnosis were recorded. We also recorded the number and location of recurrences identified at US, the distance between the dominant and nondominant recurrent tumors measured at US (in those patients with multiple recurrences), the biopsy results, and the pathologic findings of the resected breast specimens. The presence or absence of cutaneous manifestations and the presence and location of distant metastasis at the time recurrence was diagnosed also were recorded.
Despite the breast imaging section policy at our institution that mammography of the reconstructed breast is not beneficial and therefore should not be performed routinely, at the request of the clinicians mammography was performed in 12 patients to evaluate a palpable mass in the reconstructed breast. The mammograms were obtained by using GE DMR+ (GE Medical Systems, Milwaukee, Wis) or Lorad M IV (LoRad Hologic Medical Equipment, Danbury, Conn) units. The mammographic examination included craniocaudal and mediolateral oblique views of the reconstructed breast. The mammographic criteria for recurrence in the reconstructed breast included the depiction of a mass, malignant-appearing microcalcifications, a mass with microcalcification, and/or architectural distortion (12). The initial interpretation was made by the mammographer on daily clinical assignment. The images and medical reports were reviewed retrospectively and correlated with the US findings by two authors (D.G.B., J.P.) who are experienced in mammography.
US was performed in all patients by four authors (D.G.B., B.S.E., B.D.F., J.P.) and three faculty members, who combined have more than 40 years of experience in breast US and more than 30 years of experience in mammography.
The equipment used to perform breast US included a high-frequency linear-array 713-MHz transducer connected to a high-resolution scanner (XP 128, Acuson, Mountain View, Calif; Ultramark 9 HDI, Advanced Technology Laboratories, Bothell, Wash; Elegra, Siemens, Issaquah, Wash). US examination included not only a focused evaluation of the region of clinical concern but also an examination of the entire reconstructed breast to detect and characterize any additional lesions suspected of being recurrent cancers.
The US features of the recurrences were recorded by the sonographer who performed the examination and were confirmed by consensus between two authors (B.S.E., B.D.F.) in an independent retrospective analysis of the images. US features included the number, location, size, echogenicity, and shape of the lesions; the regularity and definition of the tumor margins; the sound transmission or acoustic shadow; the presence or absence of an echogenic rim; calcification; skin involvement; and tumor-associated vascularity at color power Doppler US (performed for 27 of [69%] 39 recurrent cancers). The location of the recurrence was recorded by using positions based on the hours of a clock, with the reconstructed nipple in the center and the most superior margin of the breast at the 12-oclock position. In 13 patients, the distance between the recurrence and the nipple was measured by using extendedfield-of-view technology (SieScape; Siemens) once it became available at our institution in December 1996. The measurement of this distance contributed to the reliable identification of given recurrences at follow-up US examinations performed to evaluate responses to chemotherapy and radiation therapy.
In patients with multiple recurrences, the tumor with the greatest diameter was designated the dominant recurrence. The distance between the dominant recurrent tumor and the smallest nondominant recurrent tumor in the reconstructed breast was recorded.
US criteria for malignancy included a solid hypoechoic mass with irregular margins, a taller-than-wider shape, acoustic shadowing, and intratumoral vascularity (8,13). Intratumoral vascularity was analyzed subjectively on the basis of the number and distribution of color Doppler US signals inside the tumor, with the presence of tortuous penetrating vessels considered highly suspicious for malignancy (1416).
Palpable masses were assessed with US for assistance in the differentiation of fat necrosis. The criteria for fat necrosis included a solid mass of increased echogenicity, a solid poorly defined mass with posterior acoustic shadowing caused in part by highly echogenic coarse calcifications, and a cystic mass with or without internal debris (ie, oil cyst) (17).
Recurrence was confirmed on the basis of cytopathologic and histopathlogic examination results. Cytopathologic and histopathologic specimens were obtained by means of US-guided FNAB (n = 25), palpation-guided biopsy (n = 5), or excisional biopsy (n = 1). After the skin was prepared with alcohol, US-guided FNAB was performed with a 20-gauge needle, with or without the administration of a local anesthetic agent along the planned needle track. The tip of the needle was clearly demonstrated within the recurrent tumor throughout the aspiration (18). The biopsy results were recorded.
In the patients with multiple recurrences, biopsy of the dominant recurrent tumor was performed. Biopsy of the nondominant recurrent tumor was performed at the discretion of the sonographer.
In two patients, US-guided FNAB was performed after failed palpation-guided core-needle biopsy. US-guided core-needle biopsy was performed at the discretion of the sonographer usually in cases of failed FNAB or in which a large sample needed to be retained for additional research and testing. Core-needle biopsy was performed with an 18-gauge cutting needle and an automatic biopsy device (Maxcore; Bard Urological, Covington, Ga) (19). After triggering of the automatic biopsy device, the needle was depicted to be traversing the lesion on the longitudinal and transverse sonograms (18). Four core-needle specimens were routinely obtained from each recurrent tumor resected at biopsy.
FNAB results were interpreted by the staff cytopathologist on daily clinical assignment. The core-needle biopsy and surgical excision specimens were evaluated by the staff pathologist on daily clinical assignment.
For those patients whose treatment included surgical excision, the recurrence was confirmed by means of pathologic evaluation of the specimen. Recurrences that were treated with chemotherapy and/or radiation therapy were monitored with follow-up US.
| RESULTS |
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Physical examination of the 20 reconstructed breasts revealed a palpable mass in 18 (90%) patients and an area described as focal thickening in two (10%) patients. Cutaneous manifestations in the form of peau dorange and erythema were present in one (5%) patient.
The initial clinical impression of the palpable masses was suspicious for recurrence in 11 (55%), suspicious for fat necrosis in six (30%), and suspicious for postoperative change in three (15%) of the 20 patients. Histopathologically, the palpable abnormality in the reconstructed breast was recurrence in 18 (90%) of the 20 patients. In two (10%) patients, at US a palpable mass of clinical concern was depicted as fat necrosis and a clinically occult recurrence was depicted in another quadrant.
Regarding the 12 patients who were referred for mammography, there was clinical concern that a palpable mass might be malignancy (seven patients), fat necrosis (three patients), or postoperative change (two patients). Fourteen recurrences, five (36%) of which were clinically occult, were depicted at mammography in these 12 patients.
All of the recurrences visualized at mammography had an irregular or stellate appearance that was characteristic of malignancy. Mammography depicted malignant-appearing microcalcifications associated with five (36%) of the recurrent tumors. The longest diameter of the 14 recurrences visualized at mammography ranged from 0.6 to 7.0 cm (mean, 1.9 cm ± 1.7).
The longest diameter of the 11 recurrences that were not visualized at mammography but were depicted at US in the 12 patients ranged from 0.3 to 0.9 cm (mean, 0.5 cm ± 0.2). Of these 11 recurrences, one (9%) was 0.8 cm in diameter, eight (73%) were 0.5 cm, and two (18%) were located too peripherally (11 cm from the reconstructed nipple) to be projected on the mammographic film.
The locations of the 39 recurrences visualized at US in the reconstructed breasts are listed in Table 2. The recurrences were solitary in 12 (60%) of the 20 patients and multiple in eight (40%). In the eight patients with multiple recurrences, the number of additional (ie, nondominant) recurrent tumors was one in four patients, two in two patients, five in one patient, and six in one patient. The nondominant recurrent tumors were multifocalthat is, located in the same quadrant as the dominant tumorin six (75%) of these eight patients and multicentric in two (25%) patients: in a quadrant adjacent to that of the dominant tumor in one case and in the quadrant opposite to that of the dominant tumor in the other case. The distance from the reconstructed nipple to the solitary or dominant recurrent tumor, which was recorded in 13 patients, ranged from 3 to 11 cm (mean, 7.3 cm ± 2.3) (Fig 1). The distance between the dominant and nondominant recurrent tumors (Fig 2), which was measured in seven patients, ranged from 0.2 to 7.0 cm (mean, 2.2 cm ± 2.3).
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| DISCUSSION |
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Although there is no imaging protocol that is recommended for monitoring the reconstructed breast for recurrence, during the study period at our institution, at the request of the clinician, breast imaging was performed in those patients who were referred for evaluation of a palpable mass. In these patients, the TRAM and latissimus dorsi myocutaneous flap breast reconstructions did not interfere with the mammographic or US detection of recurrence. US of the reconstructed breast enabled confirmation of clinically suspicious palpable masses as recurrences, depicted clinically occult recurrences, and enabled diagnosis of recurrence in those patients in whom the clinical impression of the palpable mass was fat necrosis or postoperative change.
It has been suggested that patient age, tumor size, and histopathologic tumor type at presentation may be factors that predispose patients to recurrence in the reconstructed breast (21). However, regarding the patients in this study, the wide ranges in age (3158 years), tumor size (0.35.5 cm), and histopathologic type at the time of presentation of the original breast cancer did not seem to support this suggestion, although the number of patients was small. The time between the diagnosis of the original breast cancer and the diagnosis of the recurrence (range, 1496 months) and the varied presentations of the original breast cancers (70% of patients had a solitary mass; 25%, multifocal masses; 5%, diffuse microcalcifications) further emphasize the difficulty in selecting a group of patients at higher risk for recurrence.
The usefulness of mammography in patients clinically suspected of having recurrent cancer in the reconstructed breast has been demonstrated (22). The mammographic appearance of recurrence has been found to be similar to that of primary breast cancer (23).
Mammographic examination of the reconstructed breast was performed without technical difficulty at our institution. The appearances of each of the visualized recurrences were typical of malignancy and thus yielded no false-positive diagnoses. The mammographic appearances of recurrence were those of spiculated or irregularly marginated masses, and the presence of suspicious microcalcifications (in five [36%] of recurrences) supported the diagnosis of malignancy. The successful mammographic detection of clinically occult recurrences (in five [36%] recurrences) in our study suggests that mammography of the reconstructed breast should be reconsidered for the early detection of recurrence.
There were some limitations in those mammographic examinations of the reconstructed breast at which recurrences that were visualized at US were not seen (11 [44%] of 25 recurrences). These limitations included difficulties in imaging recurrences at a periphery of the breast that could not be included in the field of view (18%) and in imaging recurrences 0.5 cm in diameter or smaller (73%).
There were no limitations in the US evaluation for recurrence in the patients included in this study. The success of US in the depiction of clinically occult (54%) and mammographically occult (44%) recurrences suggests the importance of US evaluation of the reconstructed breast. Furthermore, the US detection of clinically occult recurrences supports the need to perform whole-breast US rather than targeted US assessmentthat is, that limited to the region of clinical concern (24).
The depth of the recurrences from the skin caused no limitations in detection. In the one patient with skin involvement, the skin changes did not hamper US assessment. US visualization of recurrences seemed to be independent of tumor size (range, 0.27.0 cm), with the majority (54%) of recurrences being 1 cm or smaller and 33% of them measuring 0.5 cm or smaller.
The US appearances of many (87%) recurrences were similar to those of primary breast cancer, and, thus, there were no false-positive diagnoses. Some recurrences had a US appearance typical of benign lesions, including fat necrosis and postoperative fluid collection. It may be difficult to ultrasonographically differentiate recurrence from fat necrosis, especially since both of these entities may be enlarged at subsequent follow-up US examinations. Unless the lesion has a typical appearance of fat necrosis (ie, echogenic mass containing oil cyst[s]), US-guided biopsy is recommended. The vascular septa in the recurrence that was clinically and ultrasonographically diagnosed as an organizing seroma or hematoma confirm the value of color Doppler US in the assessment of any breast lesion (25). The benign characteristics of some recurrences emphasize the importance of having a heightened suspicion of malignancy regarding all solid masses that develop in reconstructed breasts.
Both palpable and clinically occult recurrences were accessible at US-guided needle biopsy, and no technical difficulties were encountered during these procedures. FNAB is sufficient for the diagnosis of recurrent malignant disease. It yielded adequate material for the accurate cytologic confirmation of malignancy of 96% (24 of 25 recurrences) of the recurrent lesions sampled. US-guided core-needle biopsy is an alternative to FNAB for the diagnosis of recurrent cancer, and it must be performed when FNAB fails to yield adequate specimens or in patients in whom additional tissue is required.
It is unclear whether the recurrence of invasive cancer in the reconstructed breast is related to systemic or local disease. In our series, the recurrences may have been related to residual mammary epithelial cells, as evidenced by the presence of residual breast parenchyma in some of the patients surgical specimens and the fact that recurrences arose directly from the residual breast parenchyma in some of these patients.
In those patients who underwent surgical intervention (85%), the procedure consisted of local excision of the recurrent nodules with conservation of the reconstructed breast. Measurement of the distance between the recurrent tumor and the reconstructed nipple performed by using extendedfield-of-view technology facilitated the preoperative identification and localization of clinically occult recurrences and thus minimized the volume of uninvolved tissue resected.
Our study results suggest that US and US-guided biopsy are valuable in the detection and histopathologic confirmation of both clinically suspicious and clinically occult recurrences in breasts reconstructed with autogenous myocutaneous flaps after mastectomy for breast cancer. A controlled study in which physical examination, mammography, and US are compared is needed to establish a protocol for following up patients after autogenous myocutaneous flap breast reconstruction for breast cancer.
| FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, B.S.E., B.D.F.; study concepts and design, B.S.E., B.D.F.; literature research, B.S.E., N.S., J.P.; clinical studies, B.S.E., B.D.F., N.S.; data acquisition, B.S.E., J.P.; data analysis/interpretation, all authors; manuscript preparation, B.S.E.; manuscript definition of intellectual content, B.S.E., B.D.F.; manuscript editing, B.D.F.; manuscript revision/review and final version approval, all authors.
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