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Published online before print October 24, 2002, 10.1148/radiol.2253011698
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(Radiology 2002;225:707-712.)
© RSNA, 2002

Breast Imaging

Local Recurrence of Breast Cancer after Breast Conservation Therapy in Patients Examined by Means of Stereotactic Core-Needle Biopsy1

Allen M. Chen, MD2, Bruce G. Haffty, MD and Carol H. Lee, MD

1 From the Departments of Diagnostic Radiology (A.M.C., C.H.L.) and Therapeutic Radiology (B.G.H.), Yale University School of Medicine, 333 Cedar St, PO Box 208042, New Haven, CT 06520-8042. Received October 16, 2001; revision requested January 10, 2002; revision received March 12; accepted May 7. Address correspondence to C.H.L. (e-mail: leec@biomed.med.yale.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate the incidence of locally recurrent breast cancer in patients treated with breast conservation surgery and radiation therapy to determine if increased local recurrence is observed in women examined by means of stereotactic core-needle biopsy (SCNB).

MATERIALS AND METHODS: Records of 551 consecutive patients with breast cancer who were treated with conservation surgery and radiation therapy were reviewed retrospectively. The 551 cases were divided into three groups: those examined by means of SCNB (n = 86), those examined by means of excisional biopsy preceded by needle localization (n = 242), and those in which the masses were palpable and who underwent biopsy without imaging guidance (n = 223). The local recurrence rate and the Mantel-Haenszel statistic for survival curves were calculated for each group. To test for statistical significance, {chi}2 analysis was performed for categorical variables and a t test or analysis of variance was performed for calculation of continuous variables.

RESULTS: With a mean follow-up of 4.9 years (range, 2.0–8.9 years), tumor recurrence rate in the SCNB group was 2.3% (two of 86), resulting in a 5-year actuarial recurrence-free rate of 0.96 ± 0.03. For the needle-localized biopsy group, recurrence rate was 5.4% (13 of 242), with a 5-year actuarial tumor recurrence-free rate of 0.88 ± 0.03. For the non–image-guided biopsy group, the recurrence rate was 10.3% (23 of 223), with a 5-year actuarial recurrence-free rate of 0.84 ± 0.03. These rates were not significantly different when the SCNB group was compared with the needle-localized biopsy group. However, the recurrence-free rate was significantly greater for the SCNB group than that for the non–image-guided biopsy group (P = .03).

CONCLUSION: In the present series to date, cancers diagnosed by means of SCNB were not associated with an increased incidence of local recurrence after breast conservation surgery and radiation therapy.

© RSNA, 2002

Index terms: Breast, biopsy, 00.1261, 00.453 • Breast neoplasms, surgery, 00.455 • Breast neoplasms, therapy, 00.47


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Public awareness of the potential benefits of screening mammography has resulted in a dramatic increase in the number of patients who present with nonpalpable mammographically detected breast abnormalities. Even though most suspicious abnormalities will ultimately prove to be benign, nonpalpable lesions have traditionally been evaluated with surgical biopsy after needle localization (1–3). In recent years, percutaneous image-guided core biopsy of the breast with large-gauge needles has gained acceptance for the diagnosis of such breast lesions. Stereotactic core-needle biopsy (SCNB) of the breast enables patients with benign disease to avoid surgery and allows for definitive preoperative planning in those with malignant disease. Results of several series show the high accuracy and reliability of this technique (4–8). Additional advantages of SCNB include minimal invasiveness, reduced cost, and shorter procedure time when compared with those of surgical biopsy (9–11).

Seeding of needle tracks with malignant cells has historically been a concern with all diagnostic needle procedures in the breast, including fine-needle aspiration biopsies and needle-localized excisional biopsies (12–14). With the expanding application of SCNB in the clinical setting, this issue has been revisited because of the widespread use of large-core needles, which, although valuable for acquiring adequate amounts of tissue for histologic assessment, also subject the tumor to more pronounced physical manipulation. Some authors have suggested that the risk from displacement of cancerous cells is theoretically increased, and they urge caution before acceptance of the technique of SCNB (15,16). Indeed, investigators who have documented tumor implantation at rates ranging from 4% to 32% after traumatic core biopsy procedures provide convincing evidence for the legitimacy of this phenomenon and naturally suggest the possibility of increased local breast cancer recurrence in women treated with conservation therapy after SCNB (17–20). In patients undergoing mastectomy after SCNB, any displaced nests of tumor cells along with the needle track itself are usually resected, thus minimizing the risks of local recurrence. However, concerns about tumor seeding and viability remain for patients who opt for breast conservation therapy. The purpose of our study was to evaluate the incidence of locally recurrent breast cancer in patients treated with breast conservation surgery and radiation therapy to determine if increased local recurrence is observed in women examined by means of SCNB.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Between July 1992 and December 1998, 551 patients with early-stage (stage 0–2) breast cancer were treated with breast conservation surgery and radiation therapy at Yale New Haven Hospital. The cancers were clinically staged in accordance with American Joint Committee and/or International Union Against Cancer guidelines. The records of these patients were reviewed retrospectively, with particular attention paid to the initial mode of pathologic diagnosis. The records were sorted as follows: nonpalpable cancers diagnosed by means of SCNB, nonpalpable cancers diagnosed by means of excisional biopsy preceded by needle localization, and palpable cancers sampled at biopsy without image guidance. For each patient, age, tumor size, estrogen and progesterone receptor status, status of surgical margins from the definitive surgical procedure, and use of adjuvant chemotherapy and/or hormonal therapy were noted. This review was approved by the hospital human investigation committee, and patient informed consent was not required.

All patients underwent lumpectomy with or without axillary node dissection, followed by external-beam radiation therapy. Breast conservation surgery typically involved excision of the tumor with a surrounding rim of normal tissue. Patients were subsequently treated with external-beam radiation therapy with a median dose of 48 Gy to the intact breast, followed by an electron beam boost to the lumpectomy site with a median dose of 64 Gy. All patients underwent treatment of the breast with use of tangential fields and routine use of medial and lateral wedges. Regional nodal radiation was delivered at the discretion of the practicing radiation oncologist, as has been previously described (21). Total dose to the regional lymph nodes, when treated, was 46 Gy, with 2 Gy per fraction. Adjuvant systemic therapy was administered as clinically indicated on the basis of patient and physician preference; patients were not routinely treated with any specific systemic therapy protocol.

Patients were clinically followed up on a 3- to 6-month schedule by the referring physician and radiation oncologists for the first few years after treatment and at least annually thereafter. Regular mammographic evaluation, usually at yearly intervals, was an integral component of the follow-up program. All patients who received a diagnosis of local recurrence underwent tissue biopsy to obtain pathologic documentation of a tumor recurrence. Patients were considered to have a local recurrence regardless of whether histologic findings of the second malignancy were the same as those of the original tumor.

Procedures
Percutaneous image-guided core biopsy was first instituted at Yale New Haven Hospital in July 1992. All core biopsies were performed with the patient on a prone dedicated table (Stereotix, LoRad, Danbury, Conn; or Universal, US Surgical, Norwalk, Conn) by one of five radiologists who were experienced in breast imaging. All of the radiologists who performed the biopsies began performing SCNB in 1992 and had the same amount of experience in this procedure during the course of this study.

Imaging findings of suspicious lesions sampled at SCNB included 39 microcalcifications and 47 noncalcified masses or densities. In 42 (49%) of the 86 SCNB procedures, an automated biopsy gun (Biopty; Bard Radiologic, Covington, Ga) with a 14-gauge needle (Biopty-Cut; Bard Radiologic) was used. In this group, the number of core specimens obtained in each case ranged from three to 10, with a mean of 6.3. In 44 (51%) of the 86 SCNB procedures, a vacuum-assisted device with an 11-gauge needle (Mammotome; Biopsys Medical, Irvine, Calif) was used. The number of core samples obtained in each case ranged from six to 20, with a mean of 11.8. In all cases, the pathology report for the SCNB samples was compared with mammographic findings by the radiologist who performed the SCNB to determine whether there was concordance. Both of these SCNB techniques have been previously described in detail (22).

Statistical Evaluation
The primary end point of interest for the present study was recurrence-free survival. All survival curve analyses were determined by using the life-table method and were calculated from the date of diagnosis to the date of death or date last seen. Follow-up duration was assessed by means of chart review and was calculated from the completion of radiation therapy to the date of death or date of last clinical examination or mammogram. All data were entered into a computerized database. Differences between categorical variables were calculated by using the {chi}2 method. Differences between continuous variables were calculated by using the t test and analysis of variance. Survival curves were calculated by means of the life-table method, and differences between survival curves were tested by using the Mantel-Haenszel test. A P value of less than .05 was considered to indicate a statistically significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Of the 551 consecutive patients with early-stage breast cancer who were treated with breast conservation surgery and radiation therapy, 86 were examined by means of SCNB, 242 by means of excisional biopsy preceded by needle localization, and 223 by means of biopsy without imaging guidance. The clinical characteristics of the patient population are outlined in Table 1. As would be expected, there were statistically significant differences in tumor size and administration of adjuvant therapy between the groups on the basis of the method of diagnosis, with patients whose cancers were initially detected by means of palpation (the non–image-guided biopsy group) having larger tumors that were treated more often with adjuvant chemotherapy and/or hormonal therapy. In addition, the patients in the non–image-guided biopsy group were significantly younger than those in the other two groups.


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  		TABLE 1. Patient Characteristics

 
Notably, no significant differences existed between the SCNB and needle-localized biopsy groups with respect to age, tumor size, or administration of adjuvant chemotherapy or hormonal therapy. Surgical margins in the SCNB group were positive for cancer significantly more often than were those in the other two groups, and tumors in the SCNB group were significantly less likely to be estrogen- or progesterone-receptor–positive.

The mean clinical follow-up for the 551 patients was 4.9 years (range, 2.0–8.9 years). For the SCNB group, mean follow-up was 4.2 years (range, 2.0–8.4 years). For the needle-localized biopsy group, mean follow-up was 5.0 years (range, 2.0–8.9 years). For the non–image-guided biopsy group, mean follow-up was 5.2 years (range, 2.0–8.9 years). Table 2 outlines the crude tumor recurrence rates (actual number of recurrences) for the 551 patients on the basis of initial mode of diagnosis. Two (2.3%) of 86 women in the SCNB group experienced tumor recurrence, resulting in a 5-year actuarial recurrence-free rate of 0.96 ± 0.03. For the needle-localized biopsy group, the crude tumor recurrence rate was 13 (5.4%) of 242, with a 5-year actuarial recurrence-free rate of 0.88 ± 0.03. For the non–image-guided biopsy group, the crude tumor recurrence rate was 23 (10.3%) of 223, with a 5-year actuarial recurrence-free rate of 0.84 ± 0.03. Except for the SCNB group versus the non–image-guided biopsy group (P = .03), these rates were not significantly different (SCNB group vs needle-localized biopsy group, P = .38; needle-localized biopsy group vs non–image-guided biopsy group, P = .07).


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  		TABLE 2. Local Breast Cancer Recurrence

 
Two patients in the SCNB group had tumor recurrences. One local recurrence was in a patient examined with the use of a 14-gauge automated gun, and one was in a patient examined with the use of an 11-gauge vacuum-assisted device. The patient who underwent SCNB with the 14-gauge automated gun received a diagnosis of a 1.0-cm invasive lobular carcinoma. Margins negative for cancer were achieved, and the patient completed radiation therapy without complications. The patient was without evidence of disease until 8 years later, when new microcalcifications were detected in the treated breast at routine mammography. The calcifications were in a different quadrant from that of the original malignancy, and results of pathologic investigation indicated ductal carcinoma in situ. Because of the different location and histologic findings of the second tumor, it was debated whether the patient experienced a true recurrence or a second primary tumor. If this case represented a second primary cancer, then the role of SCNB in contributing to this local recurrence is irrelevant.

The second patient in the SCNB group with a local recurrence had undergone SCNB with an 11-gauge vacuum-assisted device for a suspicious cluster of calcifications. Twelve cores were obtained, and intraductal and invasive ductal carcinoma, measuring a total of 2 cm in diameter, was diagnosed. The margins of the lumpectomy specimen were negative for invasive carcinoma, but ductal carcinoma in situ was present at the medial margin of excision. Three years after breast conservation therapy, the patient developed new calcifications at the lumpectomy site and received a diagnosis of ductal carcinoma in situ without evidence of invasive carcinoma.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
Concerns about tumor displacement and needle track seeding date back to the 1950s, when the safety of fine-needle aspiration biopsy of breast cancer was first questioned (12). Studies in which investigators attempted to elucidate the hazards of fine-needle aspiration biopsy appeared in the literature throughout the next several decades, and most investigators concluded that needle track seeding was a clinically rare and inconsequential complication (23–26). In an attempt to quantify the incidence of needle track seeding for all malignancies, Smith (26) surveyed findings in 470 hospitals, reviewed 63,108 aspiration biopsy records, and found only three occurrences of needle track seeding (incidence of 0.005%). However, empiric evidence from experimental analyses involving specimens from both animal and human subjects continued to suggest that the incidence of tumor deposition after fine-needle aspiration biopsy might be underestimated and clinically important (27–30).

Despite the results of these studies, which demonstrated that tumor cells are deposited along the needle track after aspiration in a large percentage of cases, it was commonly assumed that these malignant cells do not remain viable in vivo and are destroyed by the host immune system or by some other inherent mechanism. Results of subsequent animal experiments with solid tumors demonstrated that only one (0.01%) in 10,000 circulating tumor cells was able to settle and grow as a metastatic tumor deposit (31,32). Critics also pointed out that experimental models were not analogous to clinical situations in humans because the particular tumors used were highly malignant, contained minimal stroma, and lacked intracellular junctions, which allowed a sufficient number of cells to be detached easily by the needle (24,26).

With respect to fine-needle aspiration biopsy for breast cancer, it was generally believed that the human breast, with its large amounts of stromal elements and nonadhesive carcinoma cells, did not offer the proper environment for seeding and was largely immune to the prospects of epithelial displacement. The fact that nearly all published reports of tumor seeding following needle procedures involved abdominal or perineal punctures, with biologically more aggressive tumors, was particularly reassuring (15,33,34).

Even so, many clinicians recommended that the needle track be routinely excised with surgery for breast cancer (13,17). Although definitive evidence in favor of this strategy was lacking, results of a few isolated case reports managed to keep this intriguing possibility alive. In 1988, breast tumor seeding along localization guide wires was theoretically described but never substantiated (13). In 1991, Tabarra et al (35) described one fine-needle aspiration biopsy specimen with extensive intraductal carcinoma in which clusters of intact abnormal epithelial cells were present in an inflammatory background in the needle track, stimulating stromal invasion. Soon, the emergence and widespread adoption of large-gauge core needles for diagnostic purposes dramatically increased concerns about potential tumor deposition. It was argued that increasing the needle diameter exponentially increased the risks of seeding (15,16,36). In 1992, Harter et al (37) presented a case of malignant seeding of the needle track after 14-gauge core biopsy of the breast.

More recently, results of several studies (17–20) in which surgically excised specimens of breast tissue were analyzed after needle biopsy have convincingly demonstrated that traumatic displacement of benign and malignant epithelial tissue is not a rare occurrence after needle procedures in humans. Because of renewed interest, strict criteria for the definition of epithelial displacement were proposed and eventually established. To be considered displaced, cell clusters must be histologically identical to, yet appear outside of, the primary tumor mass. Moreover, these residual fragments must not be bounded by basement membrane or specialized mammary stromal tissue (20).

In the past, concern centered largely on epithelial displacement as a potential source of misdiagnosis for the pathologist, and studies focused almost exclusively on the incidence of this phenomenon (Table 3). Boppana et al (38) attempted to address the question of fine-needle aspiration biopsy causing "diagnostic difficulties" in the evaluation of breast cancer. They reported an epithelial displacement rate of 36% after 22-gauge fine-needle aspiration biopsy in 100 consecutive patients with breast cancer. Grabau et al (17) later detected carcinoma cells in the skin or subcutaneous tissue in two (4%) of 47 mastectomy specimens in which breast cancer had been diagnosed by means of 19-gauge needle biopsy. No data were given regarding the frequency or extent of epithelial displacement in breast parenchyma.


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  		TABLE 3. Incidence of Epithelial Displacement after Needle Procedures in the Breast

 
Youngson et al (18) subsequently reviewed slides from patients with breast carcinoma who underwent surgical excision following 14-gauge SCNB, and they reported tumor displacement in 12 (28%) of 43 cases. Liberman et al (19) observed tumor displacement in two (7%) of 28 cases of ductal carcinoma in situ diagnosed by means of 11-gauge vacuum-assisted SCNB and acknowledged that epithelial displacement after SCNB can lead to difficulties in histologic interpretation, specifically since displaced ductal carcinoma in situ may mimic stromal invasion.

In the largest series to date, Diaz et al (20) found that epithelial displacement occurred in 114 (32%) of 352 cases. In all cases, the displaced tumor cell clusters had the same histologic makeup as that of the primary lesion and were detected either within the needle track or in stroma immediately adjacent to the track. Furthermore, they suggested that SCNB with the 14-gauge automated gun (36%) was associated with a higher incidence of tumor displacement than that of SCNB with the 11-gauge vacuum-assisted device (23%) because of the need for multiple passes, even though no statistical significance was established.

Unlike previous studies in which investigators focused on epithelial displacement solely as a potential source of misdiagnosis, Diaz et al (20) also attempted to address the viability and biologic importance of displaced tumor cells. By analyzing the temporal relationship between time of needle core biopsy and date of surgery, they concluded that the decreasing incidence of tumor displacement at increasing intervals between core biopsy and excision provided strong evidence that the host immune system, possibly through the production of an inflammatory reaction to the biopsy procedure, is capable of eliminating any surviving nests of tumor cells.

Although the legitimacy of epithelial displacement has been well established in these well-planned and detailed studies, its biologic importance remains unclear. In particular, there is a lack of studies relating tumor seeding with clinical outcome. In our study, we aimed to address natural concerns about possible seeding of cancer cells during radiologic interventional breast procedures as a source of local recurrence. While Diaz et al (20) suggested that any displaced tumor resulting from iatrogenic manipulation of breast cancer cells disappears with time, authors of another study (18) argued the contrary. Thurfjell et al (39) presented three cases in which seeding or tumor implantation was suspected as the cause of local recurrence in patients who did not receive radiation therapy.

The results of our study demonstrate that patients who have tumors diagnosed by means of SCNB do not have an increased risk of local tumor recurrence after a mean clinical follow-up of 4.9 years if they subsequently undergo breast conservation surgery and radiation therapy. Although Diaz et al (20) suggested that rates of tumor displacement might be higher for patients who undergo SCNB with use of an automated gun rather than a vacuum-assisted device, in our study, we found no differences in local recurrence between these two patient populations.

Although tumor cell displacement after needle procedures occurs more commonly than once believed, local recurrence apparently does not occur at an increased rate in patients examined by means of SCNB. Two mechanisms have been proposed for this finding. First, the host immune system is capable of mounting a response that eradicates any residual tumor cells isolated in the stroma or along the needle track. Second, radiation therapy eliminates any surviving tumor cells that were displaced from the primary cancer. Realistically, both of these mechanisms probably contribute to reducing the risk of local recurrence, although to what extent remains undetermined. However, while it is unknown whether patients examined by means of SCNB who undergo lumpectomy without radiation therapy are at increased risk for local recurrence, results obtained from Thurfjell et al (39) suggest that this indeed may be the case. If so, postoperative radiation therapy should be prescribed for patients with breast cancer who underwent prior SCNB.

The possibility of systemic dissemination of tumor cells after needle procedures has also been suggested in previous reports (12,23). While beyond the scope of the present study, future research efforts should address this issue by analyzing the rates of distant metastases and overall survival in patients who have undergone SCNB. Displacement of tumor cells into lymphatic and vascular spaces adjacent to the needle track is not only a theoretic likelihood but has been demonstrated to occur, both with and without evidence of tumor emboli elsewhere in the specimen (20,40). The biologic and clinical importance of this phenomenon could have profound implications on overall patient care, particularly with regard to adjuvant therapy.

While increased follow-up will certainly be required, SCNB does not appear, so far, to be associated with an increased incidence of local recurrence after breast conservation surgery and radiation therapy. Despite reports of epithelial displacement and needle track seeding, local recurrence rates were not increased in patients examined by means of SCNB, and questions remain if these findings are a result of the effects of radiation therapy, the host immune response, or some other inherent mechanism.

On the basis of the results of the present series and those of Thurfjell et al (39), it can be argued that patients examined by means of SCNB should strongly be considered for radiation therapy to minimize any risks from the procedure. Although we acknowledge the limitations of our review and cannot account for bias inherent in any retrospective study, our results offer reasonable reassurances to women whose breast tumors were initially diagnosed by means of SCNB and who were subsequently treated by means of lumpectomy and radiation therapy. In conclusion, SCNB, when followed by breast conservation surgery and radiation therapy, is a clinically acceptable procedure for the diagnosis and management of early-stage breast cancer.


   FOOTNOTES
 
2 Current address: Department of Therapeutic Radiology, M.D. Anderson Hospital, Houston, Tex. Back

Abbreviation: SCNB = stereotactic core-needle biopsy

Author contributions: Guarantors of integrity of entire study, B.G.H., C.H.L.; study concepts and design, B.G.H., C.H.L.; literature research, A.M.C.; clinical studies, A.M.C., B.G.H., C.H.L.; data acquisition, A.M.C.; data analysis/interpretation, A.M.C., B.G.H.; statistical analysis, B.G.H.; manuscript preparation, A.M.C., C.H.L.; manuscript definition of intellectual content, editing, revision/review, and final version approval, C.H.L.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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