Breastcancerchoices.org

Healing is a matter of time,  but it is sometimes also a matter of
opportunity
                                            ----Hippocrates

Medical Articles
Biopsies - Part 2   

Acta Radiol. 2000 Sep;41(5):435-40. .

Local breast cancer recurrence caused by mammographically guided punctures.

Thurfjell MG, Jansson T, Nordgren H, Bergh J, Lindgren A, Thurfjell E.

Department of Oncology, Radiology and Clinical Immunology, Uppsala
University Hospital, Sweden.

PURPOSE: To evaluate the risk of needle track seeding or tumor cell
implantation as the cause of locally recurrent breast cancer after breast
conserving surgery. MATERIAL AND METHODS: We reviewed
recurrences from a consecutive series of 303 clinically nonpalpable breast
cancers treated with breast conserving surgery after pre-operative
localization. The median mammographic follow-up was 5.4 years. The
suspicion of seeding or implantation was based on the location of the
recurrent lesion in comparison with the needle path in two orthogonal
mammographic projections. Pre-operative percutaneous biopsies had
been done in 71% (214/303) of the cases. Postoperative radiotherapy was
administered to 82% (194/238) of the invasive cancers and to 28%
(18/65) of the ductal cancers in situ (DCIS). RESULTS: Locally recurrent
cancer occurred in 11% (33/303) of the cases. Radiotherapy
demonstrated a protective effect from relapse among invasive cancers but
not for DCIS. Seeding or implantation was suspected in 3 recurrent
invasive cancers which had not been subject to radiotherapy. The
histopathological diagnosis of the primary cancer and the recurrent cancer
were the same in these cases: adenoid cystic, mucinous and tubuloductal
cancer. CONCLUSION: Seeding or implantation was suspected as the
cause of local recurrence in 7% (3/44) of the invasive cancers which did
not receive radiotherapy.

Publication Types:
Case Reports
PMID: 11016762 [PubMed - indexed for MEDLINE]


Full Text article from Radiology 2002;225:707-712.


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


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, 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


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


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 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


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.


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).


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


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 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. 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). 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.


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. LOOKLOOK

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.LOOK

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.
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

Ciatto S, Cataliotti L, Distante V. Nonpalpable lesions detected with mammography: review of 512
consecutive cases. Radiology 1987; 165:99-102.[Abstract]
Hall FM, Storella JM, Silverstone DZ, Wyshak G. Nonpalpable breast lesions: recommendations
for biopsy based on suspicion of carcinoma at mammography. Radiology 1988; 167:353-
358.[Abstract]
Meyer JE, Eberlein TE, Stomper PC, Sonnefeld MR. Biopsy of occult breast lesions: analysis of
1261 abnormalities. JAMA 1990; 263:2341-2343.[Abstract]
Parker SH, Burbank F, Jackman RJ, et al. Percutaneous large-core breast biopsy: a multi-
institutional study. Radiology 1994; 193:359-364.[Abstract]
Liberman L, Dershaw DD, Rosen PP, et al. Stereotaxic core biopsy of breast carcinoma: accuracy
at predicting invasion. Radiology 1995; 194:379-381.[Abstract]
Doyle AJ, Murray KA, Nelson EW, Bragg DG. Selective use of image-guided large-core needle
biopsy of the breast: accuracy and cost-effectiveness. AJR Am J Roentgenol 1995; 165:281-
284.[Abstract]
Liberman L, Dershaw DD, Rosen PP, Cohen MA, Hann LE, Abramson AF. Stereotaxic core biopsy
of impalpable spiculated breast masses. AJR Am J Roentgenol 1995; 165:551-554.[Abstract]
Meyer JE, Christian RL, Lester SC, et al. Evaluation of nonpalpable solid breast masses with
stereotaxic large-needle core biopsy using a dedicated unit. AJR Am J Roentgenol 1996; 167:179-
182.[Abstract]
Liberman L, Fahs MC, Dershaw DD, et al. Impact of stereotaxic core breast biopsy on cost of
diagnosis. Radiology 1995; 195:633-637.[Abstract]
Israel PZ, Fine RE. Stereotactic needle biopsy for occult breast lesions: a minimally invasive
alternative. Am Surg 1995; 61:87-91.[Medline]
Burbank F. Stereotactic breast biopsy: its history, its present, and its future. Am Surg 1996;
62:128-150.[Medline]
Robbins GF, Brothers JH, Eberhart WF, Quan S. Is aspiration biopsy of breast cancer dangerous
to the patient? Cancer 1954; 7:774-778.[Medline]
Kopans DB, Gallagher WJ, Swann CA, et al. Does preoperative needle localization lead to an
increase in local breast cancer recurrence? Radiology 1988; 167:667-668.[Abstract]
Fajardo LL. Breast tumor seeding along localization guide wire tracks. Radiology 1988; 169:580-
581.[Medline]
Roussel F, Dalion J. The risk of tumoral seeding in needle biopsies. Acta Cytol 1989; 33:936-
938.[Medline]
Roussel F, Nouvet G. Evaluation of large-needle biopsy for the diagnosis of cancer. Acta Cytol
1995; 39:449-452.[Medline]
Grabau DA, Anderson JA, Gaverson HP, Dyneborg U. Needle biopsy of breast cancer:
appearance of tumor cells along the needle track. Eur J Surg Oncol 1993; 19:192-194.[Medline]
Youngson BJ, Liberman L, Rosen PP. Displacement of carcinomatous epithelium in surgical
breast specimens following stereotaxic core biopsy. Am J Clin Pathol 1995; 103:598-602.[Medline]
Liberman L, Vuolo M, Dershaw DD, et al. Epithelial displacement after stereotactic 11-gauge
directional vacuum-assisted breast biopsy. AJR Am J Roentgenol 1999; 172:677-681.[Abstract]
Diaz LK, Wiley EL, Venta LA. Are malignant cells displaced by large-gauge needle core biopsy
of the breast? AJR Am J Roentgenol 1999; 173:1303-1313.[Abstract]
Haffty BG, Fischer D, Fischer JJ. Regional nodal irradiation in the conservative treatment of breast
cancer. Int J Radiat Oncol Biol Phys 1990; 19:859-865.[Medline]
Philpotts LE, Shaheen NA, Carter D, Lange RC, Lee CH. Comparison of rebiopsy rates after
stereotactic core needle biopsy of the breast with 11-gauge vacuum suction probe versus 14-
gauge needle and automatic gun. AJR Am J Roentgenol 1999; 172:683-687.[Abstract]
Berg JW, Robbins GF. A late look at the safety of aspiration biopsy. Cancer 1962; 15:826-829.
Kline TS, Neal HS. Needle aspiration biopsy: a critical appraisal: eight years and 3267 specimens
later. JAMA 1978; 239:36-39.[Abstract]
Holm HH, Pederson JF, Kirstensen JK, Rasmussen SN, Hancke S, Jensen F. Ultrasonically
guided percutaneous punctures. Radiol Clin North Am 1975; 13:493-503.[Medline]
Smith EH. The hazards of fine-needle aspiration biopsy. Ultrasound Med Biol 1984; 10:629-
634.[Medline]
Engzell U, Esposti PL, Rubio C, Sigurdson O, Zajicek J. Investigation on tumour spread in
connection with aspiration biopsy. Acta Radiol Ther Phys Biol 1971; 10:385-398.[Medline]
Ryd W, Hagmar B, Eriksson O. Local tumour cell seeding by fine-needle aspiration biopsy: a
semiquantitative study. Acta Pathol Microbiol Immunol Scand 1983; 91:17-21.
Struve-Christensen E. Iatrogenic dissemination of tumour cells. Dan Med Bull 1978; 25:82-
87.[Medline]
Eriksson O, Hagmar B, Ryd W. Effects of fine-needle aspiration and other biopsy procedures on
tumor dissemination in mice. Cancer 1984; 54:73-78.[Medline]
Liotta LA, Kleinerman J, Saidel GM. Quantitative relationships of intravascular tumor cells, tumor
vessels, and pulmonary metastases following tumor implantation. Cancer Res 1974; 34:997-
1003.[Medline]
Schirrmacher B. Experimental approaches, theoretical concepts, and impacts for treatment
strategies. Adv Cancer Res 1985; 43:1-32.[Medline]
Moul JW, Miles BJ, Skoog SJ, McLeod DG. Risk factors for perineal seeding of prostate cancer
after needle biopsy. J Urol 1989; 142:86-88.[Medline]
Smith EH. Complications of percutaneous abdominal fine-needle biopsy. Radiology 1991;
178:253-258.[Abstract]
Tabarra SO, Frierson HF, Fechner RE. Diagnostic problems in tissues previously sampled by fine-
needle aspiration. Am J Clin Pathol 1991; 96:76-80.[Medline]
Roussel F. Risk of metastasis during fine needle aspiration (letter). J Clin Pathol 1990;
43:878.[Medline]
Harter LP, Curtis JS, Ponto G, Craig PH. Malignant seeding of the needle track during stereotaxic
core needle breast biopsy. Radiology 1992; 185:713-714.[Abstract]
Boppana S, May M, Hoda S. Does prior fine-needle aspiration cause diagnostic difficulties in
histologic evaluation of breast carcinomas? (abstr). Lab Invest 1994; 70:13A.
Thurfjell MG, Jansson T, Nordgren H, Bergh J, Lindgren A, Thurfjell E. Local breast cancer
recurrence caused by mammographically guided punctures. Acta Radiol 2000; 41:435-
440.[Medline]
Youngson BJ, Cranor M, Rosen PP. Epithelial displacement in surgical breast specimens following
needling procedures. Am J Surg Pathol 1994; 18:896-903.[Medline]