Radioactive Seed Localization of Breast Lesions: an Adequate Localization Method Without Seed Migration

ORIGINAL ARTICLE Radioactive Seed Localization of Breast Lesions: An Adequate Localization Method without Seed Migration

Tanja Alderliesten, PhD,* Claudette E. Loo, MD,* Kenneth E. Pengel, MSc,* Emiel J. Th. Rutgers, MD, PhD, Kenneth G. A. Gilhuijs, PhD,* and Marie-Jeanne T. F. D. Vrancken Peeters, MD, PhD *Department of Radiology; and Department of Surgery, The Netherlands Cancer Institute – Antoni van Leeuwenhoek Hospital (NKI-AVL), Amsterdam, The Netherlands n Abstract: Preoperative localization is important to optimize the surgical treatment of breast lesions, especially in nonpalpable lesions. Radioactive seed localization (RSL) using iodine-125 is a relatively new approach. To provide accurate guidance to surgery, it is important that the seeds do not migrate after placement. The aim of this study was to assess short-term and long-term seed migration after RSL of breast lesions. In 45 patients, 48 RSL procedures were performed under ultrasound or stereotactic guidance. In the ﬁrst 12 patients, the lesion was localized with two markers: an iodine-125 seed and a reference marker. In 33 patients, 36 RSL procedures were performed using a single iodine-125 seed. All patients received control mammograms after seed placement and prior to surgery. In the patients with two markers, migration was deﬁned as the difference in the largest distance between the markers observed in the mammograms. For single-marked lesions, migration was assessed by comparing distances between anatomical landmarks in the mammograms. RSL was successful in all patients. Seeds were in-situ for 59.5 days on average (3–136 days). The detection rate during surgery was 100%. Overall, an average seed migration of 0.9 mm (standard deviation 1.0 mm) was observed. Neither differences in lesion type, nor days in situ, type of surgery or radiologic localization method were found to have impact on seed migration. RSL is an accurate preoperative localization method for breast lesions with negligible seed migration, independent of time in-situ. n Key words: breast-conserving surgery, image-guided localization, iodine-125, migration, radioactive seed localization

reast cancer is the most common type of cancer (a) patients with nonpalpable ductal carcinoma in situ Bin women. More than one million women world- (DCIS); (b) patients with small invasive lesions; and wide are newly diagnosed with breast cancer each (c) patients who have a (near) complete response to year. neoadjuvant chemotherapy. All three patient groups Currently, breast-conserving surgery (BCS) is pre- are increasing, partly because of the aging population ferred to mastectomy when feasible. Because incom- combined with improved breast-cancer screening tech- plete excision of the lesion is a signiﬁcant risk factor nology and partly because of the more wide-spread for local recurrence and local recurrence is associated use of neoadjuvant chemotherapy. with higher mortality (1,2), it is important to mini- For the excision of nonpalpable lesions, a preopera- mize incomplete surgery. Especially nonpalpable tive localization by the radiologist is essential. Preop- breast cancer poses, however, major challenges to BCS erative localization of breast cancer is typically in this respect. The incidence of incomplete excision performed using wire-guided localization (WGL) or of nonpalpable breast cancer is higher than that of using the radioguided occult lesion localization palpable breast cancer (3,4). There are three groups of (ROLL) technique (5–12). In WGL, one or multiple patients in whom nonpalpable lesions are found: wires are placed in or surrounding the lesion to serve as a guiding tool for the surgeon. ROLL is based on 99m Address correspondence and reprint requests to: Marie-Jeanne T. F. D. an intra-lesional injection of technetium-99m ( Tc) Vrancken Peeters, The Netherlands Cancer Institute - Antoni van Leeuwen- labeled nanocolloid. Excision of the lesion is per- hoek Hospital, Department of Surgery, P.O. Box 90203, 1006 BE Amster- formed with the aid of a gamma probe that registers dam, The Netherlands, or e-mail: [email protected]. the radioactivity of the injected nanocolloid. DOI: 10.1111/j.1524-4741.2011.01155.x More recently, radioactive seed localization (RSL) 2011 Wiley Periodicals, Inc., 1075-122X/11 The Breast Journal, Volume 17 Number 6, 2011 594–601 has been proposed (13). RSL involves implanting RSL of Breast Lesions: No Seed Migration • 595

radioactive iodine-125 seeds into the lesion prior to ‘‘double-marked’’ group. The remaining patients were surgery. Similar to the ROLL procedure, a gamma assigned to the ‘‘single-marked’’ group. probe provides intra-operative guidance to locate and excise the lesion with the radioactive seed. A potential RSL & Radiologic Localization advantage of RSL over ROLL is that the seed provides Mammography and ultrasound of the breast were a small point source of radioactivity enabling accurate performed in all patients. Patients in whom the lesion guidance during surgery. RSL has been compared with was visible at ultrasonography underwent an ultra- WGL and was strongly favored over WGL (14,15). In sound-guided RSL. For this procedure, a Philips iU22 these studies, RSL was performed up to 5 days prior (Philips Healthcare, Eindhoven, The Netherlands) or a to surgery. Seed migration was not the focus of these GE ⁄ Kretz Volusion 730 (GE Medical Systems, Zipf, studies. As a result, little is known about the ability of Austria) ultrasonography unit was used. In the the seeds to migrate over longer periods of time remaining patients, stereotactic RSL was performed (5 months), e.g., when RSL is applied prior to neo- guided by X-ray mammography (XM) (Model adjuvant chemotherapy. Also, little is known which ASY-00072; Lorad Medical Systems, Danbury, CT). procedures during treatment are more likely to cause Single-packed iodine-125 seeds were used for the seed migration. Knowledge of these factors may aid to RSL procedures (Figs. 1 and 2). At the time of place- optimize the surgical margins in BCS. ment, the seeds contained on average 0.13 mCi The aim of this study is to prospectively evaluate (range: 0.03–0.21 mCi) of iodine-125. After occluding seed migration after RSL for surgery of nonpalpable the tip of a 10 cm long 18 gauge needle (item no. breast lesions, taking multivariate factors into account 15810020, Bard Peripheral Vascular – Biopsy, Tempe, including time in-situ of the iodine-125 seed. AZ) with sterile bone wax (knochenwachs W30; Johnson & Johnson, Ethicon GmbH, Germany), the radioactive seed was placed into the needle with twee- MATERIALS AND METHODS zers. Confirmation of placement of the seed in the tip of the needle was obtained via measurement with a Patient Data scintillation detector (Type 540, Mini Instruments; Between January 2008 and February 2009, 45 Stratec Services BV, Houten, The Netherlands). patients received surgery after implantation of iodine- For patient comfort, we applied local anesthesia. 125 seeds (STM1251; Bard Brachytherapy, Carol Subsequently, the radiologist placed the tip of the Stream, IL). All procedures were performed according needle in the center of the lesion. This was performed to accepted clinical indications. The radioactive seeds under ultrasound or stereotactic mammography guid- were placed for different clinical indications: prior to ance. When imaging confirmed that the tip of the neoadjuvant chemotherapy (n = 22), prior to wide needle (with iodine-125 seed and loosely placed stylet) local excision (WLE) for nonpalpable DCIS or infil- was in the center of the lesion, the seed was deployed trating ductal carcinoma (IDC) (n = 20), a diagnostic by fully advancing the stylet. After withdrawal of the excision biopsy (n = 2), and re-excision (n = 1) for needle, both the needle and the breast were residual DCIS. Patients who demonstrated favorable investigated with a scintillation detector to confirm response to neoadjuvant chemotherapy, resulting in that the seed was placed in the breast. residual lesion smaller than 3 cm, received BCS. Oth- ers underwent mastectomy. In the first 12 patients, lesions were localized with both an iodine-125 seed and a standard O-twist-marker (OTM3.OS, [diameter of ring: 3 mm, needle length: 13.7 cm, 18 gauge], Bard Peripheral Vascular – Biopsy, Tempe, AZ) to exclude potential unexpected large shifts. The markers were inserted during the same radiologic examination. In the following 33 patients, the breast lesion was localized by an iodine- Figure 1. Photograph of three iodine-125 seeds (STM1251) man- 125 seed only. All patients in whom the lesion was ufactured by Bard Brachytherapy, (Carol Stream, IL). Copyright CR localized with two markers were assigned to the Bard. 596 • alderliesten et al.

Figure 2. Product design of an iodine-125 seed. The seed has a nominal length of 4.5 mm and a nominal width of 0.8 mm. The copper layer is coated with iodine-125. The seed has a gold core and is encased in titanium. The seed has ﬂat ends. Copyright CR Bard.

To confirm correct placement and to monitor the distance between the two markers after placement potential seed migration, all patients received and after surgery. Patients in whom the initial distance mammograms (MLO and CC view) at two different between the two markers exceeded 10 mm were trans- times: (a) directly after RSL; (b) prior to surgery ferred to the group of single-marked lesions. In these (either on the day before surgery or on the day of sur- patients, differences in distance between the markers gery). For patients in the double-marked group, addi- could not be reliably attributed to seed migration tional X-ray images were acquired of the excision alone, but could also be caused by deformation of the specimen (in two orthogonal directions) after surgery. tissue in between due to differences in breast compression during mammography. This threshold was empir- Surgery ically derived based on the observations of the During surgery a handheld gamma detector radiologists. (Neo2000 Gamma Detection System, model 2200) For patients in the single-marked group, seed manufactured by Neoprobe Corporation (Dublin, migration was first assessed by clinical radiologic OH) was used to localize the iodine-125 seeds. The reading performed by an attending radiologist who 27-keV 125I gamma source was detected as a separate compared the mammograms obtained after RSL with signal from the 140-keV 99mTc source, which is rou- those obtained immediately prior to surgery. All tinely used for sentinel lymph node mapping. The con- radiologic readings of seed migration were subse- sole processed the detected gamma emissions and quently revised by one experienced breast radiologist provided audio and visual feedback to the surgeons to (C.L.) who compared the position of the seed relative locate and excise the lesion. to surrounding anatomical structures in detail in both After surgery, both the removed tissue and the exci- mammograms. sion cavity in the breast were investigated with the gamma probe to ensure removal of the seed and to Statistics exclude radioactive contamination. As the data showed deviations from normal distri- butions, nonparametric statistical analyses were per- Assessment of Seed Migration formed. We used Spearman ranked correlation to Migration of the radioactive iodine-125 seed was determine correlations between the migration and the assessed in two different patient groups. In the dou- initial distance between the two reference markers. ble-marked group, the largest distance between the Potential correlations between the migration and num- iodine-125 seed and the reference marker was assessed ber of days in situ were evaluated as well. Differences (T.A.) on the mammograms corresponding to the were considered to be statistically significant at MLO and CC views. For this purpose, a Kodak PACS p £ 0.05. workstation (Version 10.2; Carestream Health, Rochester, NY) was used. Similar measurements were also performed in the X-ray images of the excision RESULTS specimen. Migration of the seed prior to surgery was defined as the difference in the distance between the Patient Data two markers after placement and prior to surgery. The mean age of the included patients was 52 years Migration of the seed during surgery was defined as (range: 29–81 years). In total, 48 RSL procedures the difference in the distance between the two markers were performed in 45 patients. Two patients in the prior to surgery and after surgery. For completeness, double-marked group, showed a distance between the the overall migration was assessed by comparison of two markers larger than 10 mm. These patients were RSL of Breast Lesions: No Seed Migration • 597

transferred to the group with single-marked lesions. Assessment of Seed Migration Consequently, this study was ultimately conducted on In the double-marked group (n = 10), the average 10 patients in the double-marked group and 35 migration of the iodine-125 seed prior to surgery was patients in the single-marked group. 0.8 mm (standard deviation [SD]: 0.9 mm, range: 0.0– 2.8 mm). In 70% of the patients, seed migration was Imaging Data £1.0 mm (Fig. 3). During surgery the average migra- In 32 RSL procedures, the markers were placed tion was 0.5 mm (SD: 0.4 mm, range: 0.1–1.2 mm). In under guidance of ultrasonography. The remaining 16 90% of the patients, seed migration during surgery procedures were guided by stereotactic mammogra- was £1.0 mm. For the whole trajectory, a total average phy. Except for the two patients who underwent a migration of 0.9 mm (SD = 1.0 mm) was observed. An diagnostic excision biopsy procedure, the pathologic overview of the findings is given in Table 1. diagnosis was known prior to placement of the seeds. The initial distance between the two markers was In 17 RSL procedures, additional biopsies were taken. not found to be correlated with the migration prior to In these cases, placement of the marker(s) could there- surgery (Spearman ranked correlation: rs = )0.04, fore be combined with a breast biopsy procedure p = 0.9). Also the number of days the iodine-125 seed (BARD Magnum Biopsy Instrument, MG1522, 14 was in situ was not found to be significantly corre- gauge; C.R. Bard, Covington, GA). lated with the migration prior to surgery, although a trend was observed toward larger migrations over Surgery longer periods of time (rs = 0.6, p = 0.09). Similarly, At the time of surgery, the seeds were 59.5 days in migration during surgery was not correlated with the situ on average (range: 3 to 136 days). Surgery was initial distance between the two markers and the num- performed guided by seeds containing on average ber of days in situ: rs = )0.2, p = 0.6 and rs = )0.3, 0.08 mCi (range: 0.01–0.17 mCi) of iodine-125. The p = 0.4, respectively. Moreover, no difference in detection rate of the iodine-125 seeds was 100%. migration was found between patients who received Thirty-six patients underwent BCS and nine RSL under guidance of stereotactic mammography or patients underwent mastectomy. This last group con- ultrasonography. Furthermore, no difference in migra- sisted of patients who had an insufficient response to tion was found between patients who received RSL neoadjuvant chemotherapy ([ILC, infiltrating lobular for DCIS or mass lesions. In addition, no difference in carcinoma] ILC: n = 1, [IDC, infiltrating ductal carci- seed migration was found for patients who did or did noma] IDC: n = 8). not receive neoadjuvant chemotherapy prior to sur- The final pathology showed that three patients gery, indicating that chemotherapy does not have received neoadjuvant chemotherapy for ILC and 19 impact on seed migration. Furthermore, within the patients for IDC. The group eligible for WLE con- group of patients receiving neoadjuvant chemother- sisted of 15 patients with pure DCIS, one patient with apy, no significant relationship between seed migra- IDC and one patient with a combination of IDC and tion and the degree of response to neoadjuvant DCIS. Furthermore, two fibroadenomas and one intra- chemotherapy was found. mammary lymph node were found. In one patient, the In the single-marked group (n = 35), the migrations diagnostic excision biopsy revealed a benign lesion, in were found to be on the order of 1 mm or less and the other patient DCIS was identified. considered negligible (Table 2). For all patients, the Lesion excision was incomplete in 4 ⁄ 36 patients revision was in agreement with the clinical reading by (11%) after BCS. Two excisions were focally incom- the attending radiologist. An illustration of compari- plete for which no re-excision was required. One of son of the relative position of the iodine-125 seed in the two patients had multifocal IDC with an exten- surrounding anatomical structures for a patient sive component of DCIS. The other patient under- included in the single-marked group is given in Fig. 4. went BCS after neoadjuvant chemotherapy for ILC. Two excisions were extensively incomplete and required additional surgery. One of the two patients had DCIS, the other patient underwent BCS after DISCUSSION neoadjuvant chemotherapy for IDC with a lobular In this study, we prospectively evaluated migration growth pattern. of iodine-125 seeds after RSL of breast lesions. To the 598 • alderliesten et al.

Figure 3. Two MLO mammography views of a breast lesion that is marked by an iodine- 125 seed (below) as well as an O-twist- marker (top). Left: mammography acquired after placement. Right: mammography prior to surgery.

Table 1. Overview of the Migration of the Seeds Table 2. Overview of the Clinical indication of the Patients Included in the Single-Marked Group Migration (mm) Initial distance Days in situ Patient Prior to During between Days Clinical no. surgery surgery Total markers (mm) in situ Indication XM Avg Min-Max Migration

1 0.9 0.1 1.0 4.3 23 Neoadjuvant Microcalcifications 82 59–105 No 2 0.1 0.4 0.3 2.6 12 chemotherapy Mass 114.3 91–135 3 1.1 0.9 0.2 1.5 9 (n = 20) Mass, microcalcifications 115.7 106–132 4 0.1 0.2 0.3 7.1 7 Occult 106 5 0.1 0.2 0.2 6.6 32 Surrounding anatomy 112.2 102–136 6 0.0 0.6 0.6 2.9 24 O-twist-marker 5 3–7 7 2.8 0.8 3.6 8.0 74 WLE ⁄ BCS Microcalcifications 30.8 6–37 No 8 1.0 0.4 0.6 2.4 122 (n = 12) Mass 23 17–29 9 1.5 0.2 1.3 3.0 133 Mass, microcalcifications 16 10 0.0 1.2 1.1 5.4 7 Surrounding anatomy 8 Avg ± SD (mm) 0.8 ± 0.9 0.5 ± 0.4 0.9 ± 1.0 4.4 ± 2.3 44.3 ± 48.2 Two markers 20.7 4–29 Diagnostic Occult 24 No Also shown are the initial distance between the iodine-125 seed and the reference mar- excision biopsy Surrounding anatomy 13 ker and the number of days in situ. Individual numbers as well as averages (Avg) and (n =2) standard deviation (SD) are given. Re-excision Surrounding anatomy 11 No (n =1) best of our knowledge, this is the first study to quan- The structures used for the assessment of seed migration in the mammograms (XM) are shown as well as the number of days the marker was in situ. if more than one RSL pro- tify migration of iodine-125 seeds in the breast in cedure fitted a category, the minimum (Min) and maximum (Max) number of days are given in addition to the average (Avg). detail, taking multivariate factors including days BCS, breast-conserving surgery; WLE, wide local excision; XM, X-ray mammography. in situ into account. RSL of Breast Lesions: No Seed Migration • 599

Figure 4. Illustration of comparison of the relative position of the iodine-125 seed in surrounding structures (calciﬁcations) for a patient included in the single-marked group. Left: mammography acquired after placement. Right: mammography prior to surgery. The observed displacement of the seed is at the submillimeter level.

Overall, migration of the seeds was found to be compatible. Nonetheless, both cause small susceptibil- negligible (1 mm) throughout the entire treatment ity artifacts at MR imaging. Generally MRI is there- chain. Only for one patient, a somewhat larger seed fore performed before seed placement to avoid migration of 2.8 mm was observed prior to surgery. interpretation problems. A possible explanation for this outlier may be that it In the past two decades, various techniques have concerns a patient with a relatively large fatty breast. been used to localize breast lesions to guide surgeons Because of this, breast tissue is easily displaceable intra-operatively. Commonly used methods are WGL which results in a different projection. During surgery, and ROLL (5,7,12). Localization markers are typically migration was hardly observed, indicating that manip- radiologically inserted using stereotactic mammogra- ulation of the tissue during surgery does not have phy or ultrasonography guidance. A potential draw- impact on seed migration. Furthermore, analysis of back of WGL is accidental displacement of the wire the data did not indicate any particular factor in the during localization and surgery. Moreover, the orienta- treatment (initial days in situ, surgery, radiologic tion of the wire sometimes interferes with the incision localization method) that significantly influenced the the surgeon intends to make. Furthermore, because the migration of the iodine-125 seeds. wire comes outside the patient’s body, this is a very A drawback of this study is that in the assessment patient unfriendly localization method. ROLL is based of seed migration two different procedures were used on an intra-lesional injection of 99mTc-nanocolloid instead of one, i.e., for single-marked lesions distances fluid. Intra-operative localization and removal of the between anatomical landmarks were compared and lesion is subsequently performed, guided by a gamma for double-marked lesions distances between two probe (5). Various studies reported that the 99mTc markers were compared. A further complication is ROLL procedure is similarly effective or superior to that a slight rotation in a large breast may cause a WGL (6–11). Although ROLL does not restrict the shift of the anatomical landmarks. As a result of this, path of access to the lesion, enabling the surgeons to for an accurate assessment of seed migration, mam- take a direct route to the lesion, the 99mTc signal from mograms need to be acquired in exactly the same the nanocolloid is typically registered as a region with fashion. We minimized the possible influence of differ- diffuse boundaries probably due to fluid spread in the ent projections by looking at the largest distance breast tissue. Hence, some uncertainty remains about between the seed and the landmarks observed on the the precise location of the injection site. Reported rates MLO and CC mammograms. We found small seed of incomplete lesion excision range between 11% and migrations for the single-marked group indicating that 30% (6,7,10). Little is currently known about potential the landmarks did not shift substantially. leakage of the tracer into surrounding breast tissue as a Although in this study we did not use magnetic res- result of differences in breast compression during onance imaging (MRI), we would like to note that different radiologic localization methods and during similar to the O-twist-marker, the iodine-seed is MRI surgery. 600 • alderliesten et al.

An advantage of RSL over ROLL is that the seed rate comparable to the lowest reported rate for the provides a small point source of radioactivity enabling use of ROLL (11%). Although both ROLL and RSL accurate localization of the disposition site during sur- reduce the rate of positive margins when compared gery. Furthermore, seeds may be placed at different with WGL (reported excision rates are 40%), this time points prior to surgery. Moreover, our investiga- rate remains too high. Given the well-localized point tion indicates that placement of seeds directly after a source of radioactivity, minimization of incomplete breast biopsy procedure is feasible. This may facilitate surgery by the use of multiple iodine-125 seeds that clinical workflow and patient logistics compared with mark the extent of nonmass lesions instead of the cen- ROLL. ter of the lesion is expected to be a feasible approach Although the dose of the seeds used in RSL for the to further reduce incomplete excisions. This approach breast is low, in The Netherlands, RSL in the breast is subject of further study. requires authorization by the government. Further- In conclusion, RSL is a relatively new procedure more, some safety issues need to be addressed. Person- which can be adequately used to guide surgery for nel handling the iodine-125 seed are required to breast lesions. Only minor migration (1 mm) of the receive training in radiation safety. As multiple depart- iodine-125 seeds in the breast has been found. Neither ments (radionuclide laboratory, radiology, surgery, differences in days in situ, lesion type, surgery type or and pathology) are involved, it is recommended to radiologic localization method were found to have track the seed throughout the hospital with a so called significant impact on seed migration. accompaniment form. A summary concerning the logistics associated with the implementation of RSL ACKNOWLEDGMENTS for breast cancer in our hospital is given in the Appendix. The authors thank Harry Maessen, Rene Wolter- The total amount of radiation dose the patient is ink, Astrid de Fouw, Marcel Steggerda, Vanessa van exposed to (during a period of 136 days this does not Hout, and Danielle Loo for their contributions to this exceed 1 Gy) is significantly lower than that of the study. Financial support of this work was provided by radiation treatment (whole breast: 50 Gy, tumor bed the Dutch Cancer Society (Grant No. NKB 2004- area: 66 Gy) these patients will receive after surgery 3082). as part of standard treatment. Therefore, for patients, the radiation dose from the seeds is negligible com- REFERENCES pared with the post BCS radiation dose they will be exposed to. Nevertheless, based on a radiation risk 1. Harris JR, Botnick L, Bloomer WD, Chaffey JT, Hellman S. Primary radiation therapy for early breast cancer: the experience at analysis, we derived the following guidelines for The Joint Center for Radiation Therapy. 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