10.1245/ASO.2003.03.050
Annals of Surgical Oncology 10:1039-1047 (2003)
© 2003 Society of Surgical Oncology
Radioactive Seed Localization Breast Biopsy and Lumpectomy: Can Specimen Radiographs Be Eliminated?
Charles E. Cox, MD,
Ben Furman, MD,
Nicholas Stowell,
Mark Ebert,
John Clark,
Elizabeth Dupont, MD,
Alan Shons, MD,
Claudia Berman, MD,
John Beauchamp, MD,
Mary Gardner, MD,
Marla Hersch, MD,
Priya Venugopal, MD,
Margaret Szabunio, MD,
Joanne Cressman, MD,
Nils Diaz, MD,
Vesna Vrcel, MD and
Rita Fairclough, PA-C
From the Departments of Surgery (CEC, BF, NS, ME, JC, ED, AS), Radiology (CB, JB, MG, MH, PV, MS, JC), and Pathology (ND, VV, RF), Comprehensive Breast Cancer Program, H. Lee Moffitt Cancer Center and Research Institute at the University of South Florida, Tampa, Florida.
Correspondence: Address correspondence and reprint requests to: Charles E. Cox, MD, Breast Program, H. Lee Moffitt Cancer Center, 12902 Magnolia Drive, Tampa, FL 33612; Fax: 813-979-9779; E-mail: coxce{at}moffitt.usf.edu
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ABSTRACT
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Background: Wire localization (WL) is the current standard for surgical diagnosis of nonpalpable breast lesions. Many disadvantages inherent to WL are solved with radioactive seed localization (RSL). This trial investigated the ability of RSL to reduce the need for specimen radiographs and operating room delays associated with WL.
Methods: A total of 134 women were entered onto an institutional review board–approved study. RSL was performed by placing a titanium seed containing .29 to 20 mCi of iodine-125 to within 1 cm of the suggestive breast lesion. The surgeon used a handheld gamma detector to locate and excise the iodine-125 seed and the lesion.
Results: Specimen radiographs were eliminated in 98 (79%) of 124 patients. Surgical seed retrieval was 100% in 124 patients. No seed migration occurred after correct radiographical placement. A total of 26 (21%) of 124 patients required a specimen radiograph; 22 (85%) of these 26 were performed for microcalcifications.
Conclusions: After surgical removal, RSL can eliminate specimen radiographs when the radiologist accurately places the seed and the pathologist grossly identifies the lesion. If small microcalcifications are noted before surgery, then specimen radiographs may be necessary. RSL reduced requirements for specimen radiographs, decreased OR time, improved incision placement, and improved resections to clear margins.
Key Words: Biopsy • Nonpalpable lesion • 125I radioactive seeds • Specimen radiograph
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INTRODUCTION
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Significant increases in the rate of detection of nonpalpable breast lesions due to increased mammographic screening and improved imaging techniques have resulted in more lumpectomies and operative breast biopsies requiring radiographical localization. The current technique for localization and surgical excision of these nonpalpable lesions is a needle-localized breast biopsy, or wire localization (WL). A thin, hooked wire of Kopans’ or Homer’s description is placed next to the lesion by the radiologist, and the surgeon uses the wire to help guide the excision.
There are several disadvantages inherent to WL. The skin entry site of the wire is often distant from the ideal skin incision site for the surgeon. The wire may not take a direct path to the lesion. These problems result in extensive dissection, tissue removal, or possible compromise in the positioning of the skin incision. Currently, Kopans or Homer wires may be dislodged during confirmatory mammography or patient transfer.1–3 Wires can also be transected, causing intraoperative loss of guidance to the lesion, and metal fragments may be left within the breast.4 Furthermore, there are increased costs related to the x-rays needed to confirm that the lesion and accompanying wire has been excised. The intraoperative time required to transfer specimens to pathology and radiology, take a film of the specimen, and wait for interpretation and notification by a radiologist may result in prolonged anesthetic time, with the combined increases in cost and risk. Finally, external positioning of wires may result in an increased infection rate while requiring same-day positioning and removal.
A new technique using radioactive seeds to localize these nonpalpable lesions has been developed at the H. Lee Moffitt Cancer Center. Gray et al. have previously shown radioactive seed localization (RSL) to be an effective alternative to WL, without many of the shortcomings of WL.5 In that prospective, randomized trial comparing RSL versus WL, the incidence of pathologically involved margins of excision was reduced with RSL (26% vs. 57%; P = .02), and scheduling conflicts were minimized. The aim of this study was to demonstrate that RSL may eliminate the need for the specimen radiograph when (1) the radiologist has placed the seed to within 1 cm of the lesion, (2) the surgeon has identified and removed the seed without dislodging it from the tissue, and (3) the pathologist has been able to grossly identify the lesion and retrieved the seed. This elimination of a postspecimen radiograph should lead to a reduction in operative time and a more cost-effective and time-efficient alternative to WL.
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METHODS
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From March 2002 to January 2003, 146 women with nonpalpable breast lesions requiring either biopsy or lumpectomy were enrolled in a prospective study to determine the efficacy of RSL in eliminating the need for specimen radiographs. The RSL procedure was explained to them in detail, and they were enrolled in an institutional review board–approved protocol after giving informed, written consent. To comply with Nuclear Regulatory Commission guidelines for the use of sealed radiation sources (iodine-125 [125I] radioactive seeds), all diagnostic radiologists were required to undergo training and proctored placement of 10 seeds by a licensed radiation oncologist or previously trained and proctored diagnostic radiologist. Therefore, of these 146 patients, 12 received a standard WL because of scheduling of these patients when nonproctored mammographers were the only available personnel for the localization procedure. Thus, 134 women underwent RSL: these consisted of patients with nonpalpable, undiagnosed lesions undergoing excisional biopsy and those with cancer previously diagnosed by core biopsy that required localization for lumpectomy. RSL was performed by placing a titanium seed containing .20 to .29 mCi of 125I at the site of the suggestive breast lesion via an 18-gauge needle (Avid-Nit, Clearwater, FL; special needle designed for use in Moffitt Cancer Center protocol 11275) by using mammography or ultrasound guidance (Fig. 1A). 125I has a half-life of 60 days and is a 27-keV source of gamma radiation. These characteristics of 125I allow for maximal separation of peak radiation energy profiles when used in combination with 99mTc used for sentinel lymph node biopsies (Fig. 1B and 1C). Therefore, a separate signal from the 140-keV 99mTc used for lymphatic mapping can be easily detected when the handheld device is set at the 99mTc window.
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FIG. 1. (A) Placement of the radioactive seed. (B) Scan photo of peak energy profiles of iodine-125 (125I) and 99mTc. (C) Schematic diagram of peak energy profiles of 125I and 99mTc.
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The needle, with its tip occluded by sterile bone wax, is guided to the lesion with ultrasound or mammography, and a stilette is used to displace the radioactive seed and the bone wax plug into the breast parenchyma at the site of the lesion. The needle is rotated and withdrawn to release any surface tension of bodily fluids between the needle, seed, and stilette. The position of the seed is confirmed with mammography (Fig. 2) to be within 1 cm of the suggestive lesion. Within the ensuing 5 days after seed placement, the patient is taken to the operating room for excision of the lesion.
A handheld gamma probe is set to detect a 27-keV 125I source and is moved across the skin surface of the breast, marking the exact point of the highest count (Fig. 3). This point of greatest activity precisely locates the seed and lesion. The incision is made at this site, and the gamma probe is used to guide the excision of both seed and lesion (Fig. 4). Seed removal within the specimen is ensured by detection of the 125I radioactive source within the excised specimen and is reaffirmed by scanning the resultant excisional biopsy or lumpectomy cavity.
The biopsy specimen is then submitted to pathology (Fig. 5). The pathologist confirms the presence of the seed by using the handheld gamma probe, and after the margins of the biopsy specimen are inked, the tissues are cut in an attempt to identify the lesion grossly. RSL lumpectomy specimens have cytology imprints made of the margins before inking and cutting of the specimen for identification of the lesion. If gross confirmation of the lesion is not achieved, the surgeon is notified, and a specimen radiograph is obtained. The results of the specimen radiograph are then communicated to the surgeon, who re-excises the lesion if necessary. When gross confirmation of the lesion is obtained by the pathologist, the surgeon is notified, the procedure is terminated, and a final pathological diagnosis is rendered to confirm the results of the intraoperative imprint cytology. If the final pathology examination demonstrates the presence of positive surgical margins, then a re-excision is performed at a later date (Fig. 6).
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FIG. 6. Algorithm for elimination of specimen radiography; this requires the radiologist to place the seed within 1 cm of the lesion and requires the pathologist to identify the lesion grossly before the surgeon terminates the procedure. RSL, radioactive seed localization; ID, identification; STAT, immediate.
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RESULTS
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A total of 134 patients underwent RSL. Of these 134 patients, only 4 (3%) did not have the seed placed within 1 cm of the lesion, measured radiographically, and of these 4 patients, 2 had a postbiopsy specimen radiograph performed because of a lack of pathologic confirmation of the lesion. The pathologist grossly identified the lesion in the remaining two patients. All of the radioactive seeds were recovered in the specimens of these four patients. A total of 124 patients had a pathologic comment of the presence or absence of the radioactive seed, and in 10 cases, identification of the seed was not reported, although all seeds were logged as having been retrieved. Those patients who had no pathologic comment regarding seed retrieval were excluded from the study; 124 patients who underwent RSL, with 142 localized lesions, became the basis for this study. A total of 49 (39.5%) of 124 patients had their radioactive seeds placed by ultrasound, and 75 (60.5%) of 124 patients had seeds placed by mammography. Eighteen patients either had 
2 lesions or required 2 seeds to bracket the lesion, thus requiring placement of 146 seeds. No migration of the radioactive seed was observed between seed placement and removal, during patient transfer, during recompression of the breast during post–seed placement mammograms, or during breast massage as related to lymphatic mapping.
The pathologist identified the radioactive seed in 145 (99.3%) of 146 seed placements; 1 seed was dislodged by the surgeon after specimen removal and was separately submitted. The lesion was grossly identified in 105 (73.9%) of 142 cases (Fig. 7).
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FIG. 7. This figure describes how many of the seeds could be retrieved by the surgeon and the pathologist in RSL patients and how many required specimen radiographs.
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One end point of the study was to validate which lesions were identified grossly by the pathologist and which required specimen radiographs. Of 31 lesions not identified grossly by the pathologist, 24 (77.4%) were microcalcifications, 6 (19.4%) were masses, and 1 (3.2%) was a biopsy clip; all of these nonidentified lesions required specimen radiographs. For 93 patients whose lesions were identified grossly by the pathologist, 56 (60.2%) were masses, whereas 25 (26.9%) were microcalcifications and were seen or accounted for at the time the specimen was cut. On a patient-by-patient basis, 24 (49%) of 49 patients with microcalcifications did not have their lesions grossly identified by the pathologist, whereas only 6 (9.6%) of 62 patients with masses were missed, and 1 patient’s clip (7.6%) out of 13 went undetected (Fig. 8).
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FIG. 8. A study end point was to determine which lesions the pathologist could identify. This figure describes which lesions did and did not require specimen radiography. Microcalc, microcalcification.
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Specimen radiographs were performed in 32 (22.5%) of 142 lesions and 26 (21%) of 124 patients. Moreover, 110 (77.5%) of 142 lesions found in 98 (79%) of 124 patients did not warrant a specimen radiograph because of gross identification of the lesion. Specimen radiographs for microcalcifications accounted for 28 (87.5%) of 32 lesions found in 22 (84.6%) of the 26 patients who required specimen radiographs. However, 31 (28.2%) of 110 lesions found in 28 (28.6%) of 98 patients who did not require specimen radiographs had microcalcifications as the primary diagnostic finding, and evidence of these microcalcifications or evidence of a previous biopsy site with no residual microcalcifications was observed by gross pathologic confirmation (Fig. 9).
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FIG. 9. This figure describes the radioactive seed localization (RSL) patients who required specimen radiographs. Most (79%) did not, and those who required the radiographs did so primarily (84.6%) because of microcalcifications (Microcalcs).
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RSL for an excisional breast biopsy was performed on 75 (52.8%) of 142 lesions in 61 (49.2%) of 124 patients, whereas 64 (45.1%) of 142 lesions in 60 (48.4%) of 124 patients underwent RSL lumpectomy. These patients who received RSL for lumpectomy originally had their disease diagnosed by stereotactic core biopsy in 52 (86.7%) of 60 cases. The remaining eight patients (13.3%) originally had their disease diagnosed by excisional biopsy but had additional mammographic lesions that required removal at the time of definitive surgery. Three patients had mastectomies in which RSL was performed because of a change in patient preference, but this aided the pathologist in detection of the nonpalpable mammographic lesions. RSL for excisional biopsy required a specimen radiograph in 26 (34.7%) of 75 lesions and in 19 (31.1%) of 61 patients, whereas RSL lumpectomies required specimen radiographs on only 6 (9.4%) of 64 specimens, or 6 (10.0%) of 60 patients (P < .02; Fig. 10).
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FIG. 10. This figure shows the breakdown of the procedures performed. Specimen radiographs were more commonly required for excisional biopsies than for lumpectomies. Microcalc, microcalcification.
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In the previous prospective, randomized report of RSL versus WL by these authors,5 a significant reduction in RSL margin re-excision was noted over that of WL lumpectomies. Therefore, this was an end point of this study: to confirm the rate of positive margins requiring re-excision when compared with the previously published results. RSL lumpectomy was performed on 64 of 142 lesions, and 38 (59.4%) of 64 required no re-excision of surgical margins. The remaining 26 (40.6%) RSL lumpectomies had surgical margins re-excised. A total of 12 of 26 surgical margins were detected by intraoperative imprint cytology; 9 of these were re-excised at the primary procedure, thus negating the need for a second surgery, whereas 3 (25%) persisted in demonstrating close (<1 mm) or positive margins on final pathology, despite negative intraoperative cytology. The remaining 14 of 26 lesions that required re-excision were initially negative by imprint cytology, yet on final pathology they were positive or <1 mm from the margin and required re-excision at a later date. Therefore, the overall results demonstrated that 47 (73.5%) of 64 lumpectomies did not require a second surgery, whereas 17 (26.5%) of 64 lumpectomies did require re-excision at a later date.
RSL excisional biopsy performed in 75 of 142 lesions revealed 55 (71.7%) with benign lesions, whereas 20 (28.3%) had confirmed malignant disease (Table 1). Of those 20 malignancies, 8 (40%) demonstrated positive margins after RSL excisional biopsy. This compares favorably to previously published reports of 51% to 60% of patients who had positive margins after WL breast biopsies6,7 (Fig. 11).
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TABLE 1. Frequency of residual disease on re-excision of malignant breast lesions investigated by radioactive seed localized breast biopsy
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FIG. 11. Margin evaluation for radioactive seed localization (RSL) is compared between lumpectomy and excisional biopsy. Included are both final pathology and imprint cytology (IC+) findings. RSL margin excision rates compare favorably to margin excision rates for wire localization.
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DISCUSSION
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Overall, the use of RSL enabled elimination of the specimen radiograph for 110 (77.5%) of 142 lesions in 98 (79%) of 124 patients in this study. Results from this study show that when the seed is placed within 1 cm of the lesion before surgery and when the pathologist identifies the mass or density grossly after identifying the seed, the specimen radiograph may be eliminated. The exception is microcalcifications. In our series, specimen radiographs for microcalcifications accounted for 28 (87.5%) of 32 of cases that required specimen radiographs.
This study also verifies the findings of the earlier randomized prospective study by Gray et al.,5 which demonstrated a significant decrease in the number of re-excisions required for RSL biopsies and lumpectomies compared with standard WL. These findings confirm the results of the previous study, which demonstrates that RSL excisional biopsy and RSL lumpectomy are more efficient methods of resection because of the lower incidence of pathologically involved margins.
Use of the seed offers improved localization compared with WL. Seed dislodgement is rare in contrast to the wire, which can be moved or dislodged during post–wire placement mammography, during patient transfer, or during breast massage before SLN biopsy. There were no incidences of seed migration during RSL biopsy or lumpectomy that resulted in loss of localization. The surgical incision can be placed directly over the lesion with the shortest distance to the lesion. Furthermore, because the seed is a point source of radiation, it allows for a constant three-dimensional spatial localization, with the ability of constant reorientation of the seed/lesion with the gamma probe during the resection procedure.
Furthermore, RSL placement may be scheduled at the radiologists’ convenience, and RSL cases can be scheduled as the first case of the day in the operating room. Because the seed is internalized within the breast and can be safely placed up to 5 days before surgery, one sees improved operating room scheduling and elimination of costly delays, which occur with same-day WL placement.
Removing the need for transporting the specimen to the radiology department before pathologic evaluation reduces operating room time and anesthetic exposure and their attendant costs. Likewise, cases can be postponed without a need for relocalization procedures or immediate wire removal.
The results of this study position RSL as an attractive alternative to WL by reducing the likelihood of errors for all medical personnel involved in the patient’s management. The RSL technique allows for more defined responsibilities and reduced liabilities in the localization, removal, and confirmation of breast lesions. The diagnostic radiological placement of the radioactive seed allows the radiologist and mammography staff flexibility of timing and positioning, directional needle placement, and a reduced concern for wire migration during compressed placement views. This gives the needed time and flexibility to validate the preoperative placement of the seed to within 1 cm of the breast lesion. Aside from eliminating wire migration by recompression of the breast for placement films, manual massage for lymphatic mapping does not alter localization because the seed is internalized completely. In addition, the seed is visible on ultrasound, and this allows for the use of ultrasound in its placement. Multiple seeds can be placed and all easily retrieved with the aid of the gamma probe. Extreme posterior placement of the seed may elude mammographic detection but can be detected easily with the gamma probe.
The liability for surgeons and pathologists with seed/lesion retrieval is greatly reduced. Problems with retained wire fragments or loss of localization due to cutting the wire are eliminated with RSL. In the unlikely event that a seed were cut into fragments during surgery, there would be no loss of localization, because part of the radioactive seed would remain to direct localization of the lesion. In addition, fragments could be easily located because all fragments contain a radioactive source. This advantage would eliminate additional localization procedures to remove metal fragments and would reduce the liability of the placement team. To date, 100% of the seeds used to localize breast lesions have been detected and removed. The seeds can be easily detected in the pathology laboratory with the use of the gamma probe, and the pathologist does not have to speculate as to the location of the lesion if the seed has not been dislodged. Furthermore, specimen radiographs can be used as a contingency, when required.
Similar techniques using radioguidance have been developed. De Cicco et al.8 describe the use of a radioguided occult lesion localization (ROLL) technique in which macroaggregated albumin tagged with Tc99 is used to localize nonpalpable breast lesions. The ROLL technique uses the same radioactive isotope that is used for lymphatic mapping, thus making it available only for diagnostic biopsy. RSL uses 125I, an isotope with different characteristics from Tc99, and can be used in conjunction with Tc99 for removal of the breast lesion and sentinel lymph node biopsy. The ROLL technique does not offer the same flexibility in scheduling that is offered by RSL; the ROLL technique must be performed within a few hours of the procedure because of diffusion and half-life of the isotope. The radiolabeled albumin cannot be seen on specimen radiographs or on ultrasound after injection, and in 12% to 15% of cases it diffuses into the tissues, negating its functional capacity to localize the lesion.
Smith et al.9 reported on the use of another effective procedure in which iatrogenically produced hematoma is used to localize the biopsy site. The lesions, along with the hematoma, are removed by using intraoperative ultrasound guidance, and subsequent confirmation of removal can be performed with ultrasound. We concur that ultrasound-guided biopsy affords significant similar advantages when compared with WL, but during the conduct of this study, ultrasound was unavailable to the surgeons on a routine intraoperative basis. RSL could be used as an adjunct to ultrasound for preoperative localization of lesions. Furthermore, RSL provides a pinpoint radiation source to which the surgeon can constantly reorient the excision with the aid of the gamma probe, which is not always possible with ultrasound-guided biopsy after the initial biopsy incision. These observations may form the basis for a randomized, prospective comparison of RSL versus ultrasound-guided excision of lesions.
Bimston et al.10 have also demonstrated that specimen radiography is not beneficial in the management or outcome of patients undergoing image-guided needle-localized breast biopsies. However, most breast surgeons routinely obtain specimen radiographs to ensure complete removal of the lesion in question. Even though specimen radiographs rarely change patient care, they are still routinely performed. Not obtaining a specimen radiograph when performing a WL breast biopsy or lumpectomy is medicolegally unsound. If the radiologist correctly places the radioactive seed, then RSL allows the surgeon to verify removal of the lesion in question by verifying that the radioactive seed is contained in the specimen, thereby negating the need for a specimen radiograph in most cases.
Drawbacks to the RSL technique are protean. The RSL technique requires training of many health-care professionals in the handling, placement, and removal of radioactive seeds. The nuclear regulatory bodies require training in their use by diagnostic radiologists. The diagnostic radiologists may be required to have a specific number of supervised placements before Food and Drug Administration (FDA) approval of a diagnostic seed can be obtained.
Some radiation safety issues have to be addressed when this innovative technique is performed. Personnel who handle the seed will be required to have some minimum training in radiation safety and may be required to use radiation-monitoring badges. The pathology staff will have to log in each seed retrieved and account for all radioactive seeds. Because this radioactive seed is implanted in the body, it requires the same regulatory mechanisms as those associated with brachytherapy, no matter how small the dose.
There are some potential risks involved with RSL, but these adverse events happen less frequently than those seen in WL or other localization techniques. Surgical instruments could inadvertently sever the seeds. The 125I used is chemically bound to a silver matrix within the seed, so the radioactive material would remain with the fragments of the seed and would not dissipate into the environment or into the bloodstream of the patient. The cut fragments could then be easily detected, removed, and calibrated for loss of any radioactivity into the environment. The patient could then be monitored for thyroid uptake of the radioactive iodine.
Other unlikely events could occur, such as inadvertently dropping the seed on the floor, into the operative field, or into the clothing of personnel. The seed could be suctioned into the suction container. The accounting of seeds in pathology would help to alert the operating staff that a seed had been misplaced, and proper location and retrieval procedures could be followed. All of these events have occurred, and the seeds have been easily located with the standard gamma probe or by monitoring Geiger counters.
The training of surgeons can be performed in conjunction with the training already received for sentinel node mapping. This training includes radiation safety training for the use of isotopes and the gamma detection device that is used for both RSL and the combination lymphatic mapping technique.
The cost of the seed is slightly higher than the cost of the wire used for WL. Seeds cost approximately US$40, whereas the needle wire system costs approximately US$20. However, the seeds could theoretically be reused if cleaned and re-sterilized. The decrease in OR time by 15 to 30 minutes because of the elimination of 79% of postspecimen radiographs makes RSL a more economically viable alternative to WL. The elimination of a postspecimen radiograph eliminates the need and time for a radiologists’ interpretation and the resultant operating room costs. RSL makes economic sense when compared with other localization techniques.
The delivery system used for RSL is a standard 18-gauge thin-walled seed-placement needle but is much shorter than the system used for prostate seed implantation. The needles must also be specifically manufactured for institutional review board–approved protocols until the FDA approves the seed for diagnostic use. There is the possibility of using smaller 20-gauge seeds compared with the standard 18-gauge seeds, which would help increase patient comfort and would provide an even more precise point source for the excision of nonpalpable breast lesions.
Although protean difficulties exist for the implementation of RSL, all but four are actually overcome by the extant methods of operation in the community of surgeons already performing lymphatic mapping for breast cancer. These four hurdles are training of the diagnostic radiologists, logging of the seeds by the pathologists, FDA approval of the seeds for diagnostic purposes, and development of a combined needle/seed delivery device for seed application.
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CONCLUSIONS
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RSL of breast lesions is an effective and cost-efficient method of localizing breast lesions. Most specimen radiographs can be eliminated, and this results in decreased operative and anesthesia time. RSL breast biopsies and lumpectomies are also more effective at eliminating the need for margin re-excisions, as seen in the lower incidence of positive margins. The radioactive seed provides a precise detection point, around which the surgeon can continually reorient the location of the lesion by using the handheld gamma detection probe.
The equipment, training, and understanding of handling radioactive materials for RSL are extant in the community of surgeons who perform lymphatic mapping and sentinel lymph node biopsy with radioactive materials. The RSL procedure is an effective, efficient method and provides a technological advance for the resection of nonpalpable lesions.
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FOOTNOTES
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Radioactive seed localization (RSL) of nonpalpable breast lesions eliminates the need for specimen radiographs in most patients, except those with microcalcifications. RSL seems to be an effective means of reducing the incidence of positive surgical margins when compared with wire localization.
Received for publication March 8, 2003.
Accepted for publication August 5, 2003.
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REFERENCES
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C. E. Cox, B. Furman, E. L. Dupont, J. W. Jakub, N. Stowell, J. Clark, and M. Ebert
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Ann. Surg. Oncol.,
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ABSTRACT
INTRODUCTION
