 |
|
Manipulation of the Primary Breast Tumor and the Incidence of Sentinel Node Metastases From Invasive Breast Cancer
Nora M. Hansen, MD;
Xing Ye, MS;
Baiba J. Grube, MD;
Armando E. Giuliano, MD
Arch Surg. 2004;139:634-640.
ABSTRACT
| |
Hypothesis The incidence of sentinel node (SN) metastases from invasive breast cancer might be affected by the technique used to obtain biopsy specimens from the primary tumor before sentinel lymph node dissection.
Design Prospective database study.
Setting The John Wayne Cancer Institute.
Patients and Methods We identified 663 patients with biopsy-proven invasive breast cancer who underwent sentinel lymph node dissection between January 1, 1995, and April 30, 1999. Patients were divided into 3 groups based on type of biopsy: fine-needle aspiration (FNA), large-gauge needle core, and excisional. A logistic regression model was used to correlate tumor size, tumor grade, and type of biopsy with the incidence of SN metastases.
Results Of the 676 cancers, 126 were biopsied by FNA, 227 by large-gauge needle core biopsy, and 323 by excisional biopsy before sentinel lymph node dissection. Mean patient age was 58 years (range, 28-96 years), and mean tumor size was 1.85 cm (range, 0.1-9.0 cm). In multivariate analysis based on known prognostic factors, the incidence of SN metastases was higher in patients whose cancer was diagnosed by FNA (odds ratio, 1.531; 95% confidence interval, 0.973-2.406; P = .07, Wald test) or large-gauge needle core biopsy (odds ratio, 1.484; 95% confidence interval, 1.018-2.164; P = .04, Wald test) than by excision. Tumor size (P<.001) and grade (P = .06) also were significant prognostic factors.
Conclusions Manipulation of an intact tumor by FNA or large-gauge needle core biopsy is associated with an increase in the incidence of SN metastases, perhaps due in part to the mechanical disruption of the tumor by the needle. The clinical significance of this phenomenon is unclear.
INTRODUCTION
The management of early-stage breast cancer has evolved during the past century to new and less invasive methods of detection, diagnosis, and treatment. The most commonly used biopsy methods to detect breast cancer are fine-needle aspiration (FNA), large-gauge needle core biopsy, excisional breast biopsy, and incisional breast biopsy. Each of these procedures has advantages that may make it the most suitable for a particular patient. In the past, a 1-step approach to the diagnosis and surgical management of breast cancer was used; if biopsy of a palpable mass demonstrated a carcinoma, a mastectomy was performed at the same time. This approach assumed that any delay in treatment might negatively affect prognosis and that the biopsy might result in tumor dissemination. Today, a 2-step approach is recommended; biopsy is followed by definitive surgical management at a later date.
Before the 1970s, mastectomy was the only curative surgical option for breast cancer. With the advent of breast conservation as an equivalent option to modified radical mastectomy with respect to overall survival,1-2 a 2-step approach now allows the patient to become more involved in her own management decisions. Retrospective and prospective clinical trials3-6 have reported no difference in the survival rates between 1- and 2-step procedures, and the interval between biopsy and definitive surgery is not related to prognosis.
During the past decade, axillary lymph node dissection for staging has been replaced by the less invasive and more accurate technique of sentinel lymph node dissection (SLND), which has changed the field of surgical oncology. As first described by Morton et al7 for patients with melanoma, the sentinel node (SN) concept is based on the fact that the afferent lymphatic channel draining the primary tumor courses first to an SN in that specific regional lymphatic basin. In 1994, Giuliano et al8 modified SLND for the staging of early breast cancer. Since then, intraoperative lymphatic mapping and SLND for breast cancer has emerged as a less invasive, more accurate staging procedure.9-10 Several SLND operative techniques have been successful in breast cancer.11-15
Because of reports of tumor displacement with different types of biopsies,16 we evaluated the incidence of SN metastases in patients undergoing FNA, large-gauge needle core biopsy, or excisional breast biopsy before SLND. We hypothesized that the type of biopsy might affect the incidence of SN metastases.
METHODS
Between January 1, 1995, and April 30, 1999, patients with biopsy-proven invasive breast cancer and clinically negative axillary lymph nodes were entered into various prospective studies of SLND. If the SN contained no evidence of tumor, completion axillary lymph node dissection was not performed. If the SN contained tumor cells, axillary lymph node dissection was recommended and performed unless the patient refused further surgery. All patients signed an informed consent form in accordance with the ethics standards of the joint Saint John's Health Center/John Wayne Cancer Institute institutional review board and in compliance with the Helsinki Declaration. Patients with primary tumors larger than 5 cm by physical examination or mammography, multicentric tumors, locally advanced disease, ductal carcinoma in situ, or stage IV disease when first seen were excluded. Also excluded were patients who underwent more than 1 type of biopsy for diagnosis of breast carcinoma.
Patients underwent breast biopsy at the Joyce Eisenberg Keefer Breast Center, John Wayne Cancer Institute at Saint John's Health Center, or were first seen with a biopsy-proven diagnosis of cancer from an outside facility. All biopsies were FNA, large-gauge needle core, or excisional. Slides from outside facilities were reviewed by our pathologists to document carcinoma before SLND. Fine-needle aspiration was performed with a 23- or 25-gauge needle. Core biopsy was performed by the surgeon using a handheld technique or ultrasound guidance or by the breast imaging service using stereotactic or ultrasound guidance. An 11- or 14-gauge needle was generally used for stereotactic biopsies, with an average of 12 core samples; a 14-gauge needle was generally used for ultrasound core biopsies, with an average of 6 core samples. The exact needle size and number of core samples were not documented for this study.
Intraoperative lymphatic mapping and SLND was performed after a breast-conserving procedure or mastectomy. In most cases, the sole mapping agent was a vital blue dye (1% Lymphazurin blue dye; U.S. Surgical, Norwalk, Conn); in selected cases, blue dye was used with technetium Tc 99m sulfur colloid. If a radioisotope was added, it was injected either the day before or the morning of the SLND procedure, and a lymphoscintigram was obtained.
Evaluation of the primary tumor was performed by the Pathology Department at Saint John's Health Center, and all original biopsy slides were reviewed. Sentinel nodes were step sectioned and stained at each level with hematoxylin-eosin. If the hematoxylin-eosin stains did not reveal metastases, the nodal sections were stained by cytokeratin immunohistochemistry (IHC) with a monoclonal anticytokeratin antibody cocktail (Zymed Laboratories Inc, South San Francisco, Calif). Nodal metastases were stratified according to the American Joint Committee on Cancer (AJCC) staging effective during the treatment, based on the 5th edition of the AJCC Cancer Staging Manual. A micrometastasis was a tumor deposit measuring 2 mm or less on hematoxylin-eosin staining; a macrometastasis was a tumor deposit larger than 2 mm on hematoxylin-eosin staining; and an IHC metastasis was a group of tumor cells identified only with IHC stains.
Univariate and multivariate logistic regression models were used to correlate tumor size, tumor grade, and type of biopsy with the incidence of SN metastases.
RESULTS
Between January 1, 1995, and April 30, 1999, 663 patients with 676 invasive, clinically node-negative, biopsy-proven breast carcinomas underwent SLND at the Joyce Eisenberg Keefer Breast Center, John Wayne Cancer Institute at Saint John's Health Center. The mean age of the patients was 58 years (range, 28-96 years). Most of the cancers (58%) were palpable on physical examination. Infiltrating ductal carcinoma accounted for 85% of cases, whereas infiltrating lobular cancer was identified in 15% of cases.
Of the 676 carcinomas, 126 were diagnosed by FNA, 227 by large-gauge needle core biopsy, and 323 by excisional biopsy. The mean tumor size was 1.85 cm (range, 0.1-9.0 cm). The mean tumor size was largest in the FNA group (2.08 cm) and smallest in the excisional group (1.63 cm) (Table 1). Although our exclusion criteria excluded patients with tumors larger than 5 cm on physical examination or mammogram, some patients did have pathologic tumors larger than 5 cm that had been underestimated by physical examination or radiologic workup. These patients were included in the study.
|
|
|
|
Table 1. Number of Cancers and Mean Tumor Size by Biopsy Group
|
|
|
Most patients underwent breast conservation (83%) instead of mastectomy (17%). Overall, the tumors in this study had favorable prognostic markers. Most tumors were estrogen receptor–positive (83.5%), progesterone receptor–positive (63.0%), and epidermal growth factor receptor–negative (70.6%).
Sentinel node macrometastases, micrometastases, or IHC-detected metastases were identified in 39% of cases. The incidence of SN metastases was 47% in the FNA group, 45% in the large-gauge needle core group, and 32% in the excisional group. This was not surprising because the size of the primary tumor was larger in the FNA group than in the excisional group.
The SN(s) was the only positive node(s) in 61% of patients in the FNA group; 39% of patients had non-SN metastases, with a range of 1 to 16 positive non-SNs. The SN(s) was the only positive node(s) in 63% of patients in the core group and 69% of those in the excisional group, with a range of 1 to 21 and 1 to 20 positive non-SNs, respectively. The presence of non-SN metastases and the number of positive non-SNs did not correlate with the biopsy type.
Of 59 metastases detected in the FNA group, 15 (25%) were IHC metastases, 7 (12%) were micrometastases, and 37 (63%) were macrometastases. Of 101 metastases detected in the core group, 27 (27%) were IHC metastases, 24 (24%) were micrometastases, and 50 (50%) were macrometastases. A similar trend was seen in the excisional group, where 35 of the 103 SN metastases (34%) were detected by IHC, 24 (23%) were micrometastases, and 44 (43%) were macrometastases. In each biopsy group, the rate of macrometastases was higher than the rate of IHC-detected metastases or micrometastases (Table 2).
|
|
|
|
Table 2. Incidence and Size of SN Metastases by Biopsy Group
|
|
|
The median interval between biopsy and the SLND procedure was 15 days overall (range, 1-232 days), corresponding to a median interval of 9.5 days for the FNA group, 16.0 days for the large-gauge needle core group, and 17.0 days for the excisional group. Some patients underwent neoadjuvant chemotherapy, which delayed the definitive surgical procedure, and other patients chose to delay their surgical intervention. The time from biopsy to SLND procedure was not significantly correlated with the presence of SN metastases (P = .29).
To determine whether the type of biopsy affected the incidence of SN metastases, a stepwise procedure was used to find the multivariate logistic regression model. This model was then used to correlate tumor size, tumor grade, and type of biopsy with the incidence of SN metastases. Univariate analysis demonstrated that tumor size, tumor grade, and type of biopsy independently correlated with the incidence of SN metastases (Table 3). Multivariate analysis based on known prognostic factors demonstrated that the incidence of SN metastases independent of age, tumor size, and tumor grade was higher in patients whose cancer was diagnosed by FNA or large-gauge needle core biopsy than by excisional biopsy. This difference was greater and statistically significant in the large-gauge needle core group vs the excisional group (P = .04) (Table 4).
|
|
|
|
Table 3. Results of Univariate Analysis
|
|
|
|
|
|
|
Table 4. Results of Multivariate Analysis
|
|
|
To determine whether the type of biopsy affected the size of SN metastases, a multivariate logistic regression model was used to correlate tumor size, tumor grade, and type of biopsy with the size of SN metastases: macrometastases vs micrometastases and IHC metastases. In the FNA group vs the excisional group, a statically significant difference was noted; however, it favored the presence of macrometastases rather than the expected micrometastases and IHC metastases. In the large-gauge needle core group vs the excisional group, there was no statistical difference between type of biopsy and the size of SN metastases.
COMMENT
A suspicious mass identified during physical examination or by mammography or ultrasonography should be biopsied to determine whether it is cancerous. Large-gauge needle core, FNA, and excisional breast biopsies are safe and reliable diagnostic tools. Major complications, such as bleeding and infection, are rare and can often be treated in the outpatient setting.17-18 The type of biopsy chosen depends on the type, location, size, and palpability of the lesion and on the preference and experience of the individual performing the biopsy.
The use of FNA dates back to the 1930s, when it was first described for diagnosing breast lesions by Martin and Ellis.19 Its introduction was a response to concern that surgical excisional biopsy might lead to dissemination of tumor cells.20 For more than 60 years, FNA has been an established procedure for the diagnosis of breast lesions in Europe, and it has become a more accepted approach in the United States in the past 30 years.21-23 Fine-needle aspiration is an easy and reliable way to diagnosis breast cancer in the palpable lesion. It is quick, relatively painless, and inexpensive. In a study and review24 of 3000 palpable breast lesions, FNA had a sensitivity of approximately 87%. However, its accuracy is highly dependent on the cytopathologist; a review22 of 31 340 FNAs demonstrated sensitivities ranging from 65% to 98% and specificities ranging from 34% to 100%. False-negative rates (reportedly 0%-4%) are often due to sampling errors and are more common in small, well-differentiated carcinomas and lobular carcinomas.25-26 Kline et al27 reviewed 3545 breast aspirates: in half of the false-negative cases, the needle tract did not extend into the tumor; most of these tumors measured less than 1 cm. Among experienced cytopathologists, a false-positive result is rare (0%-0.4%).28-29
Diagnostic large-gauge needle core biopsy is a safe and effective alternative to FNA or excisional biopsy.30-33 A core biopsy sample allows a more detailed histologic interpretation that can more completely characterize the lesion and often distinguish between invasive and noninvasive disease. Core biopsy can be performed using manual palpation, ultrasound guidance, or a stereotactic approach. Because needle sizes ranging from 11 to 18 gauge allow collection of larger specimens, insufficient specimens are uncommon. The biopsy sample is evaluated by a pathologist rather than a cytopathologist, which obviates the need for personnel specially trained in cytopathology and permits the evaluation of tumor architecture. Sensitivity and specificity rates are high for large-gauge needle core biopsy. In one study,34 a 79% accuracy rate was reported, with no false-positive results. In another study,35 a sensitivity of 89% increased to 94% in lesions larger than 2.5 cm. Large core samples obtained using 14-gauge cutting needles improve sensitivity, specificity, and overall diagnostic accuracy compared with FNA or smaller core samples.36-37
For breast cancer and other tumors, FNA carries a theoretical risk of tumor seeding, but the incidence of needle tract seeding is low.38 Seeding of the needle tract and mechanical displacement into the lymphatic or vascular system has been documented in breast cancer, but the clinical implications are not known.39-41 None of these studies documented a survival disadvantage with FNA.
In an animal study, Ryd et al42 performed FNA in solid and ascites-growing mouse tumors. The incidence of "successful tumor takes" was a function of the number of cells seeded after FNA and was in the range of 103 to 104 cells. Tumor seeding of the core biopsy needle tract has been reported in several series, but again the clinical significance of these findings is not known. The incidence of tumor seeding has been shown to increase with larger needle diameters.43-44 Diaz et al45 reported a 32% incidence of tumor cell displacement after large-gauge needle core biopsy; the incidence and amount of tumor displacement was inversely related to the interval between core biopsy and excision, suggesting that displaced tumor cells do not survive displacement. Other researchers46 report a diagnostic dilemma with displaced tumor cells in the breast stroma owing to large-gauge needle core biopsy, particularly in patients with noninvasive cancer. Several studies have evaluated the impact of core biopsy on local recurrence. In a study by Chao et al,47 2 cases of subcutaneous breast cancer recurrence at the stereotactic biopsy site were identified 12 and 17 months after definitive treatment of the primary breast tumor. An additional patient underwent excision of the skin and dermis at the time of mastectomy, and tumor cells were identified in the dermal scar. All 3 patients had undergone a stereotactic core biopsy with multiple passes of a 14-gauge needle followed by modified radical mastectomy. Other studies48-49 have not documented an increase in local recurrence rates.
Few studies have examined lymph node findings after needle biopsies. Carter et al16 described histologic findings in axillary lymph node dissections performed 2 weeks after needle core biopsy (n = 3) or excisional biopsy (n = 12). All breast excision specimens showed evidence of previous surgical manipulation, and 3 specimens contained displaced cellular fragments in the lymphovascular spaces next to the needle track. Each case had breast-derived epithelial cells in the subcapsular sinus of a draining lymph node; however, in 4 cases these epithelial cells were not from the breast cancer. The authors concluded that previous surgical or needle manipulation could cause mechanical transport of tumor or normal breast epithelium to the subcapsular sinus of the lymph node and that these displaced cells do not have a negative effect on prognosis.
The results of the present study indicate that the type of biopsy is associated with differences in the incidence of SN metastases. We agree with Carter et al16 that nodal metastases may reflect mechanical manipulation and disruption of the tumor by the biopsy needle, but no statement can be made regarding whether these metastases would eventually impact regional recurrence or overall survival. Fidler and Hart50 showed that a growing primary tumor contains heterogeneous populations of cells, some of which are highly metastatic. Tumor cell dissemination is thought to occur shortly after primary tumor vascularization, and most metastases from a primary breast cancer are initiated when the primary tumor is smaller than 0.125 cm.51 Although mechanical disruption might facilitate the lymphatic transport of metastatic cells, the successful colonization and growth of these cells in a draining lymph node is a highly complex process. If tumor-host interactions do not favor the development of clinically relevant metastasis, mechanical disruption might well prove to be prognostically unimportant.
Many breast cancer studies have attempted to document the significance of occult nodal metastases identified by evaluation of multiple sections and IHC stains. The results of these studies are conflicting, and the true significance of these metastases remains unknown.52 The American College of Surgeons Oncology Group recently completed accrual to the Z0010 study, which was designed to evaluate the significance of micrometastases in the SN or the bone marrow of patients with invasive breast cancer. It is hoped that the results of this study will finally address the significance of micrometastases in the regional lymph nodes of patients with invasive breast cancer. In the meantime, further investigation is needed to confirm our observation that the type of biopsy is associated with the incidence of SN metastases. Until this observation can be further evaluated and validated, we do not plan on changing our practice patterns, which presently incorporate the use of FNA, large-gauge needle core biopsy, and excisional biopsy in the management of breast lesions.
AUTHOR INFORMATION
| |
Corresponding author: Nora M. Hansen, MD, Joyce Eisenberg Keefer Breast Center, John Wayne Cancer Institute at Saint John's Health Center, 2200 Santa Monica Blvd, Santa Monica, CA 90404 (e-mail: hansenn{at}jwci.org).
Accepted for publication February 17, 2004.
This study was supported by the Ben B. and Joyce E. Eisenberg Foundation, Los Angeles, Calif; the Fashion Footwear Association of New York Charitable Foundation, New York; the Leslie and Susan Gonda (Goldschmied) Foundation, Los Angeles; the John Wayne Cancer Institute Auxiliary, Santa Monica; the Rabinovitch Foundation, Beverly Hills, Calif; and the Witherbee Foundation, Santa Monica.
This paper was presented at the 111th Scientific Session of the Western Surgical Association; November 10, 2003; Tucson, Ariz; and is published after peer review and revision. The discussions that follow this article are based on the originally submitted manuscript and not the revised manuscript.
From the Joyce Eisenberg Keefer Breast Center, John Wayne Cancer Institute at Saint John's Health Center, Santa Monica, Calif. Dr Grube is now with the Department of Surgery, The University of Texas Medical Branch, Galveston.
REFERENCES
1. Fisher B, Anderson S, Bryant J, et al. Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med. 2002;347:1233-1241.
FREE FULL TEXT
2. Veronesi U, Cascinelli N, Mariani L, et al. Twenty-year follow-up of a randomized study comparing breast conserving surgery with radical mastectomy for early breast cancer. N Engl J Med. 2002;347:1227-1232.
FREE FULL TEXT
3. Jackson PP, Pitts HH. Biopsy with delayed radical mastectomy for carcinoma of the breast. Am J Surg. 1959;98:184-189.
FULL TEXT
|
ISI
| PUBMED
4. Abramson DJ. Delayed mastectomy after outpatient biopsy: long-term survival study. Am J Surg. 1976;132:596-598.
FULL TEXT
|
ISI
| PUBMED
5. Fisher ER, Sass R, Fisher B. Biologic considerations regarding the one and two step procedures in the management of patients with invasive carcinoma of the breast. Surg Gynecol Obstet. 1985;161:245-249.
ISI
| PUBMED
6. Bertario L, Reduzzi D, Piromalli D, et al. Outpatient biopsy of breast cancer: influence on survival. Ann Surg. 1985;201:64-67.
ISI
| PUBMED
7. Morton DL, Wen DR, Wong JH, et al. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg. 1992;127:392-399.
8. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220:391-401.
ISI
| PUBMED
9. Giuliano AE, Dale PS, Turner RR, et al. Improved axillary staging of breast cancer with sentinel lymphadenectomy. Ann Surg. 1995;222:394-399.
ISI
| PUBMED
10. Giuliano AE. Mapping a pathway for axillary staging: a personal perspective on the current status of sentinel lymph node dissection for breast cancer. Arch Surg. 1999;134:195-199.
FREE FULL TEXT
11. Borgstein PJ, Pijpers R, Comans EF, et al. Sentinel lymph node biopsy in breast cancer: guidelines and pitfalls of lymphoscintigraphy and gamma probe detection. J Am Coll Surg. 1998;186:275-283.
FULL TEXT
|
ISI
| PUBMED
12. Klimberg VS, Rubio IT, Henry R, et al. Subareolar versus peritumoral injection for location of the sentinel lymph node. Ann Surg. 1999;229:860-865.
FULL TEXT
|
ISI
| PUBMED
13. Linehan DC, Hill ADK, Akhurst T, et al. Intradermal radiocolloid and intraparenchymal blue dye injection optimize sentinel node identification in breast cancer patients. Ann Surg Oncol. 1999;6:450-454.
ABSTRACT
14. Albertini JJ, Lyman GH, Cox C, et al. Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA. 1996;276:1818-1822.
ABSTRACT
15. Krag DN, Weaver DL, Alex JC, Fairbank JT. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol. 1993;2:335-339; discussion 340.
FULL TEXT
|
ISI
| PUBMED
16. Carter BA, Jensen RA, Simpson MD, et al. Benign transport of breast epithelium into axillary lymph nodes after biopsy. Am J Clin Pathol. 2000;113:259-265.
FULL TEXT
|
ISI
| PUBMED
17. Nguyen M, McCombs M, Ghandehari S, et al. An update on core needle biopsy for radiologically detected breast lesions. Cancer. 1996;78:2340-2345.
FULL TEXT
|
ISI
| PUBMED
18. Dershaw D, Liberman L. Stereotaxic breast biopsy indications and results. Oncology. 1998;12:907-916.
PUBMED
19. Martin HE, Ellis EB. Biopsy by needle procedure and aspiration. Ann Surg. 1930;92:169-181.
PUBMED
20. Silver CE, Koss LG, Brauer RJ, et al. Needle aspiration cytology of tumors at various body sites. Curr Probl Surg. 1985;22:1-67.
ISI
| PUBMED
21. Franzen S, Zajicek J. Aspiration biopsy in diagnosis of palpable lesions of the breast: critical review of 3479 consecutive biopsies. Acta Radiol Ther Phys Biol. 1968;7:241-262.
ISI
| PUBMED
22. Hermans J. The value of aspiration cytologic examination of the breast: a statistical review of the medical literature. Cancer. 1992;69:2104-2110.
FULL TEXT
|
ISI
| PUBMED
23. Zajdela A, Ghossein NA, Pilleron JP, et al. The value of aspiration cytology in the diagnosis of breast cancer: experience at the Foundation Curie. Cancer. 1975;35:499-506.
FULL TEXT
|
ISI
| PUBMED
24. Masood S. Occult breast lesions and aspiration biopsy: a new challenge. Diagn Cytopathol. 1993;9:613-614.
ISI
| PUBMED
25. Wollenberg NJ, Caya JB, Clowry LF. Fine needle aspiration cytology of the breast: a review of 321 cases with statistical evaluation. Acta Cytol. 1985;29:425-429.
ISI
| PUBMED
26. O'Malley F, Casey TT, Winfield AC, Rodgers WH, Sawyers J, Page DL. Clinical correlates of false-negative fine needle aspirations of the breast in a consecutive series of 1,005 patients. Surg Gynecol Obstet. 1993;176:360-364.
ISI
| PUBMED
27. Kline T, Joshi L, Neal H. Fine needle aspiration of breast: diagnosis and pitfalls. Cancer. 1979;44:1458-1464.
FULL TEXT
|
ISI
| PUBMED
28. Innes DJ Jr, Feldman PS. Comparison of diagnostic results obtained by fine needle aspiration cytology and Tru-Cut or open biopsies. Acta Cytol. 1983;27:350-354.
ISI
| PUBMED
29. Smallwood J, Herbert A, Guyer P, et al. Accuracy of aspiration cytology in the diagnosis of breast disease. Br J Surg. 1985;72:841-843.
ISI
| PUBMED
30. Kopan DB, Gallagher WJ, Swann CA, et al. Does preoperative needle localization lead to an increase in local breast recurrence? Radiology. 1988;167:667-668.
FREE FULL TEXT
31. Burbank F. Stereotactic breast biopsy: comparison of 14- and 11-gauge mammotome probe performance and complication rates. Am Surg. 1997;63:988-995.
ISI
| PUBMED
32. Janes RH, Boutin MS. Initial 300 consecutive stereotactic core-needle breast biopsies by a surgical group. Am J Surg. 1994;168:533-536.
FULL TEXT
|
ISI
| PUBMED
33. Fentiman I, Millis R, Hayward J. Value of needle biopsy in outpatient diagnosis of breast cancer. Arch Surg. 1980;115:652-653.
ABSTRACT
34. Minkowitz S, Moskowitz R, Khafif R, et al. Tru-cut needle biopsy of the breast: an analysis of its specificity and sensitivity. Cancer. 1986;57:320-323.
FULL TEXT
|
ISI
| PUBMED
35. Parker SH, Lovin JD, Jobe WE, et al. Stereotactic breast biopsy with a biopsy gun. Radiology. 1990;176:741-747.
FREE FULL TEXT
36. Parker SH, Lovin JD, Jobe WE. Nonpalpable breast lesions: stereotactic large-core biopsies. Radiology. 1991;180:403-407.
FREE FULL TEXT
37. Harter LP, Curtis JS, Ponto G, et al. Malignant seeding of the needle track during stereotaxic core needle breast biopsy. Radiology. 1992;185:713-714.
FREE FULL TEXT
38. Smith EH. Complications of percutaneous abdominal fine-needle biopsy: a review. Radiology. 1991;178:253-258.
FREE FULL TEXT
39. Youngon BJ, Cranor M, Rosen PP. Epithelial displacement in surgical breast specimens following needle procedures. Am J Surg Pathol. 1994;18:896-903.
ISI
| PUBMED
40. Tabara SO, Frierson HF, Fechner RE. Diagnostic problems in tissues previously sampled by fine-needle aspiration. Am J Clin Pathol. 1991;96:76-80.
ISI
| PUBMED
41. Sneige N, Singletary SE. Fine-needle aspiration of the breast: diagnostic problems and approaches to surgical management. Pathol Annu. 1994;29(pt 1):281-301.
42. Ryd W, Hagmar B, Eriksson O. Local tumour cell seeding by fine-needle aspiration biopsy: a semiquantitative study. Acta Pathol Microbiol Immunol Scand A. 1983;91:17-21.
ISI
| PUBMED
43. Grabau DA, Andersen JA, Graversen HP, et al. Needle biopsy of breast cancer: appearance of tumour cells along the needle. Eur J Surg Oncol. 1993;19:192-194.
PUBMED
44. 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.
ISI
| PUBMED
45. 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.
FREE FULL TEXT
46. Douglas-Jones AG, Verghese A. Diagnostic difficulty arising from displaced epithelium after core biopsy in intracystic papillary lesions of the breast. J Clin Pathol. 2002;55:780-783.
FREE FULL TEXT
47. Chao C, Torosian MH, Boraas MC, et al. Local recurrence of breast cancer in the stereotactic core needle biopsy site: case reports and review of the literature. Breast J. 2001;7:124-127.
FULL TEXT
| PUBMED
48. King TA, Hayes DH, Cederbom GJ, et al. Biopsy technique has no impact on local recurrence after breast-conserving therapy. Breast J. 2001;7:19-24.
FULL TEXT
| PUBMED
49. Chen AM, Haffty BG, Lee CH. Local recurrence of breast cancer after breast conservation therapy in patients examined by means of stereotacti |
