- Email: [email protected]
Fine needle aspiration cytology versus percutaneous biopsy of nonpalpable breast lesions
European Journal of Radiology 42 (2002) 10 – 16 www.elsevier.com/locate/ejrad
Fine needle aspiration cytology versus percutaneous biopsy of nonpalpable breast lesions M. Meunier a,*, K. Clough b a
Department of Radiology, Institut Curie, 26 rue d’Ulm, 75231 Paris Cedex 05, France Department of Surgery, Institut Curie, 26 rue d’Ulm, 75231 Paris Cedex 05, France
b
Received 27 November 2001; accepted 28 November 2001
Abstract Fine needle aspiration (FNA) and core biopsy (CB) are efficient alternatives to surgical biopsy: FNA provides a sampling of cells and is very cost effective. The main limits are insufficient sampling rate and the impossibility to diagnose invasion. CB allows architectural description and the diagnosis of specific benign and malignant lesions, but is more expensive and time-consuming. © 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Breast cancer; Fine needle aspiration; Percutaneous biopsy
1. Introduction In the last two decades, the diagnostic radiologist has gradually evolved from a passive interpreter of the mammogram to a physician who participates actively in the diagnosis of breast cancer. This evolution began with the expansion of fine needle aspiration (FNA) cytology under sonographic and stereotactic guidance. Percutaneous biopsies, primarily core biopsy (CB) developed later and were rapidly considered as an alternative to surgical biopsy. FNA provides a sampling of cells (cytological material). Percutaneous biopsies yield a large core of tissue in which the architectural description and tissue elements recognition is possible (histology material) with the diagnoses of specific benign and malignant lesions. These interventional procedures reduce the number of unnecessary excisional biopsies for benign lesions and lower the false positive cases and cost of screening. CB replaces frozen section during lumpectomy. Axillary dissection in most institutions is performed only for invasive carcinomas. In doing so, cancer surgery will * Corresponding author. Tel.: +33-1-4432-4200; fax: + 33-1-44324015. E-mail address: [email protected] (M. Meunier).
necessitate only a one step surgery for treatment, instead of a two step surgery: one for diagnosis and one for treatment.
1.1. Objecti6e To compare, contrast and analyze the value and limitations of FNA and percutaneous biopsies.
2. Techniques
2.1. Fine needle aspiration cytology FNA is performed with a 20–23 gauge needle, which is often attached to a syringe. Once the needle is introduced into the lesion, negative pressure is applied by pulling back on the syringe, allowing the aspiration of material for sampling. Numerous multidirectional passes through the lesion increase the probability of successful sampling, especially in small lesions. The cellular material is preserved on slides for interpretation by the cytopathologist. FNA is accomplished in a relatively short period of time. Sampling of different lesions is easily feasible.
0720-048X/02/$ - see front matter © 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 7 2 0 - 0 4 8 X ( 0 1 ) 0 0 4 8 0 - 6
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
2.2. Percutaneous biopsy CB is performed with a specially designed 14–18 gauge needle that is placed in an automated biopsy gun. Once the needle is positioned at the appropriate depth, the spring loaded gun rapidly advances into the lesion, taking a core of tissue during its excursion. At least four or five passes through the lesion are needed. CB allows a monodirectional sampling of the target. This inconvenience is compensated by aspiration with the vacuum assisted device, which allows harvesting of larger quantity of tissue with a single needle insertion. After targeting, while the suction is on, specimens are obtained by rotating the aperture of the bowl clockwise with 2 h increments. Roughly 1 cm3 of tissue is removed when 12 specimens are done per tour. Both are performed under stereotactic or sonographic guidance. Depending on the modality of guidance used, a percutaneous biopsy requires 30 min to 1 h to perform. Histological samples are preserved in formalin for interpretation by a histopathologist.
3. Results There is no strict criteria for reporting cytologic results. FNA can be reported as malignant, suspicious for carcinoma, benign or insufficient specimen. A standardized uniform terminology into five categories (unsatisfactory, benign, indeterminate/atypical, suspicious/probably malignant and malignant) has been recommended by The National Cancer Institute [1]. FNA cannot make the diagnosis of invasive carcinoma; in most institutions frozen section at the time of lumpectomy is still required before planning lymph node dissection. Advantages of percutaneous biopsy over FNA are: the accurate diagnosis of specific benign and malignant lesions; the recognition of a specific benign lesion and differ-
11
entiation between true negative specific benign lesion and false negative result due to sampling error; the differentiation between invasive and noninvasive cancers; tumor grading.
3.1. Fine needle aspiration cytology Data from published series are difficult to compare because study designs, techniques and cases selection differ significantly. There are no strict criteria for classification of atypia or suspicious lesions. Surgical biopsy is recommended for suspicious lesions because a nonnegligible percentage will turn out to be malignant. Table 1 presents the results of FNA with surgical correlation.
3.2. Percutaneous biopsy Numerous studies and a recent meta-analysis were published [6]. Preset inclusion criteria were: nonpalpable lesion; all histological diagnoses of CB specimens had to be confirmed by either surgical biopsy or 2 years follow-up; the absolute number of benign and malignant diagnoses had to be derivable; a minimum of at least five cores had to be obtained. A total of 865 CB were done, the overall sensitivity was 97%, 3% false negative, the malignancy rate varies between 23 and 57%. Despite benign CB results, authors insist upon the impact of breast cancer prevalence of the lesions detected by screening and referred for biopsy. In a population: with a low prevalence of malignancy e.g. 20%, the probability of cancer being present despite benign CB is low: 0.6%. with a prevalence of 50% the probability of carcinoma being present will still be 3%.
Table 1 Results of FNA with sugical correlation Authors
Guidance
Total (ratio B/M)
NS
True negative
True positive
False negative
False positive
Azavedo et al. [2]
Stereotactic
567 (138/429)
49 27 cancers
102 (20%)
285 (55%)
117 (22%)
14 (3%)
Meunier et al. [3]
Stereotactic
228 (103/125)
59 34 cancers
74 (44%)
86 (51%)
7 (4%)
4 (2%)
Sneige et al. [4]
Ultrasound
254 (83/168)
27 12 cancers
65 (29%)
152 (67%)
4 (2%)
4 (2%)
Thibault et al. [5]
Ultrasound
174 (79/95)
14 6 cancers
66 (41%)
80 (50%)
9 (6%)
5 (3%)
12
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
4. Diagnosis accuracy
4.1. FNA The false negative cases are attributed to sampling errors, specimen quality or to characteristics of the lesion: infiltrating lobular carcinoma or marked desmoplasia. In a series from 4455 FNA of palpable masses, 41 false negative aspirations were reviewed. No interpretation errors were identified. Twenty-one FNA (51%) were classified as adequate (8– 100 well preserved cells) and 20 FNA (48%) as inadequate (less than six cells). Cases of invasive lobular carcinoma were more common in the false-negative smears with inadequate sampling [7]. FNA in experienced hands, has a reported false positive rate around 2%, very close to frozen section examination. After conservative treatment, radiationinduced changes can be interpreted as recurrent carcinoma. Of the 49 suspicious tumors reported by Sneige 38 (76%) were found to be malignant. Eleven (22.4%) were benign after excisional biopsy: two mucocelelike lesions, one nipple adenoma, one adenosis, three ductal hyperplasia and three fibroadenomas [8]. Apocrine cysts with alarming cytologic atypia can be misinterpreted as carcinoma. Proliferative breast disease includes hyperplasia without atypia, hyperplasia with atypia and carcinoma in situ. The diagnosis of these lesions is important in identifying women at an increased risk for breast cancer: the risk is 1.5 to 2-fold for proliferative lesions without atypia, 4 to 5-fold with proliferative lesions with atypia and 8 to 10-fold with carcinoma in situ. With the increased use of FNA, cytopathologists are often asked to differentiate such entities and depending on the threshold chosen the rate varies from 2 to 22% [9,10]. Cytologic findings of atypia in FNA samples should prompt excisions, 61% of these cases proved malignant [11]. Cytopathologists have tried to establish different criteria [12,13] and insist on architectural features [14]. Interobserver variability in classification of proliferative breast lesions has been reported, exact cytohistologic correlation being achieved in only 36% of cases [15].
4.2. Percutaneous biopsy Burbank and Parker introduced a method to evaluate the accuracy and the quality of an image-guided breast biopsy program [16]. The histologic diagnoses of CB and surgical specimens are classified in four categories: benign disease; high risk lesions: atypical ductal hyperplasia, lobular carcinoma in situ, atypical lobular hyperplasia and radial scar; ductal carcinoma in situ; infiltrating carcinoma.
The miss rate is the percentage of all cancers diagnosed as benign by CB; it is estimated around 3%. A lesion is concordant when pathology is the same for CB and lumpectomy. Benign lesions are followed and if stable are classified as benign. A lesion is overestimated when upgraded by CB. A lesion is underestimated when a lower degree of pathology is described at CB than at lumpectomy. This group is divided in two categories: the DCIS underestimated rate defined as the percentage of DCIS on CB upgraded in invasive carcinoma on lumpectomy; the ADH underestimated rate, defined as the percentage of ADH on CB that is upgraded to DCIS or invasive. ADH are classified with underestimated lesions and not as false negative cases, because open surgery is recommended, specially if all the target had been removed. For percutaneous biopsy, underestimation seems related to the effect of biopsy device, to probe size, mammographic lesion type, lesion size and number of samples.
4.2.1. CB may fail to show in6asi6e carcinoma In a multicentric study, the rate of underestimation of DCIS was 20.4% for lesions diagnosed at CB and 11.2% of lesions diagnosed at vacuum-assisted biopsy. DCIS underestimation was 1.9 times more frequent with masses than with calcifications, 1.8 times more frequent with CB than with vacuum-assisted biopsy, and 1.5 times more frequent with ten or fewer specimens per lesion than with more than ten specimens per lesion [17]. 4.2.2. CB may fail to show DCIS For lesions diagnosed initially as atypical ductal hyperplasia, underestimation of DCIS and invasive ductal carcinoma was significantly less frequent using the 11gauge directional vacuum-assisted device compared with the 14-gauge directional vacuum-assisted device (19 vs. 39%, P= 0.025) and with the automated 14gauge needle (19 vs. 44%, P= 0,01) [18]. Finally, the underestimation rate for calcifications was 16.3% (14/ 86) and 1.6% (1/64) for masses. No underestimation was found if the entire lesion was removed at vacuum suction biopsy [19]. Lobular carcinoma in situ (LCIS) is an incidental finding, occult mammographically. When the pathologic results shows only LCIS, surgical excision is usually recommended because the mammographic target may be missed and breast cancer is often associated with LCIS nearby. Benign or malignant papillary lesions are accurately diagnosed with CB in the majority of the cases, but cases diagnosed as suspicious for malignancy or with atypia or unusual associated histologic findings should be excised.
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
Radial scars often appear as areas of architectural distortion and are frequently associated with carcinoma. Carcinoma is more frequent when the size of the radial scar is more than 5 mm or patients older than 40 years. It has generally been advised that radial scar should be excised surgically; when diagnosed at CB surgery is still recommended.
5. Prognostic factors FNA and CB are being used increasingly as the initial diagnostic procedure. Clinicians are interested in obtaining as much prognostic information as possible from these limited specimens. FNA material can be evaluated for specific biochemical molecular markers including steroid hormone receptor status, flow cytometry to determine DNA content (ploidy) and the percentage of cells that are in the growth portion of the cell cycle (S-phase fraction). CB specimens allow immunohistochemical assessment of estrogen and progesterone receptor status, c-erbB-2 and p53 [20]. Tumor cellularity is evaluated by counting cells within one high power field. For invasive carcinomas, tumor size, histologic grade, lymphatic invasion, and extensive intraductal carcinomas are important prognostic factors. Histologic grade between CB and surgical specimens are discordant in 25% of cases. Inversely the evaluation of tumor size, lymphatic vessel invasion and intraductal component is severely limited in CB specimens [21].
13
the lesion; but vacuum-assisted biopsy can remove a small target. The goal of percutaneous breast biopsy is diagnosis, not treatment. Complete removal of a target does not ensure complete excision of the histologic abnormalities. Residual carcinoma was found in 75% of 15 carcinomas in which the target was removed by 11-gauge vacuum-assisted biopsy [23]. The rational for removal of most the mammographic abnormality is to compensate for sampling error and underestimation. After total excision of microcalcifications, a radioopaque clips should be left in place because histology can turn out to be malignant and preoperative needle localization impossible. Furthermore, a complete removal of a target might decrease the anxiety of patients and in young patients would have a consequence on the rhythm of follow-up.
6.3. Needle track seeding The displacement of malignant cells away from the target has been described with FNA, CB or wire localization [24–26]. There is no evidence that the displaced epithelium is viable, however, it can lead to histologic interpretation errors: displaced DCIS can mimic infiltrating ductal carcinoma. The frequency of epithelial displacement after 14-gauge CB is reported to be higher than after directional vacuum-assisted biopsy [27]. Longterm follow-up of cancers diagnosed by percutaneous biopsy is necessary to determine the significance of needle track seeding on local recurrence and survival.
6.4. Insufficient specimens rate 6. Limits and controversies
6.1. Targeting When seen sonographically, masses are best reached under ultrasound guidance. Fine needle position or pre-fire and post-fire needle should be shown on films. Under stereotactic guidance good lesions conspicuity on stereotactic pairs of images obtained before and during the procedure and needle positions on the pre-fire and post fire position should be documented. Architectural distortions are very difficult to target because they change on pair images. The target can be displaced or masked by hemorrhage or xylocain. For microcalcifications, specimen radiography is needed to confirm the quality of sampling. The resolution of current digital systems is still inferior to that on screen-film techniques: as a result, subtle microcalcifications can be difficult to target. Finally, in 16% of cases, cancers are found near but at a distance from the targeted microcalcifications [22].
6.2. Complete excision 6ersus sampling With FNA and CB, diagnosis is made by sampling of
For nonpalpable breast lesions, the insufficient samples rate of FNA varies between studies. In a multicentric trial, the overall insufficient sampling rates were 40% for stereotactic guidance and 8.45% for ultrasound guidance [28]. This difference can be partly explained by the modality of sampling: multidirectional by ultrasound guidance and monodirectional with stereotactic guidance. FNA that yields insufficient specimens add to the costs of screening because patients usually have to go onto excisional biopsy. The most effective way to reduce insufficient specimen rates is to have a cytopathologist who can immediately stain and microscopically evaluate the smears, additional aspirations being performed immediately when necessary. In contrast to FNA, CB produces few insufficient samples.
7. Follow-up Cytologic diagnoses must be correlated with the clinical and imaging findings (the triple test) to reduce the rate of false-negative cases, but concordant benign triple tests do not entirely exclude the possibility of
14
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
carcinoma, and such cases require periodic follow-up. Noncompliance of half of the patients with follow-up recommendations is an important issue undermining the benefits of FNA [29]. Because CB is a sampling rather than an excisional technique, the issue of patient follow– up after the procedure has been raised. Parker proposes follow–up mammography at 6 months for benign biopsy results concordant with the imaging findings and annual screening if no significant change is evident [30]. Brenner proposes follow-up mammograms at 6, 12, 24 and 36 months [31]. The appropriate interval and duration of follow-up in different situations needs further assessment and clarification. Compliance of patients to follow-up remains an important concern. In a national survey the reported time for follow-up was 12 months [32].
8. Multidisciplinary approach Close collaboration of a multidisciplinary team is necessary in managing patients after image guided breast biopsy procedures. Radiologists should consider what histologic diagnoses they will accept for every abnormalities biopsied. When pathologic results are congruent with the radiologic abnormalities, follow-up is proposed. If pathologic results show no evidence of malignant tumor but the radiologic lesion is highly suspicious, after review of needle position and samples, preoperative needle localization is recommended.
9. Socio-economic outcome
9.1. Lower the cost of screening Screening mammography is believed to reduce breast carcinoma mortality for women aged over 50 years. Since mammographic findings are nonspecific, and although in most cases it is possible to differentiate between benign and malignant abnormalities, large numbers of breast biopsies for benign lesions are generated. It has been estimated that 11– 30% of screening mammography disclose nonpalpable lesions, 1– 5% lead to a biopsy and 0.5% of abnormalities will reveal a cancer [33]. The positive biopsies vary between 30 and 60% in Europe and 10 and 30% in the USA. Approximately 32% of the total cost of breast carcinoma screening is due to open surgical biopsy for benign lesions [34]. FNA cytology and percutaneous biopsy are noninvasive, cost effective procedures. They allow a rapid determination of the nature of equivocal lesions and relief of anxiety of patient, eliminating 4– 6 months followup. For many women with benign breast disease,
surgery is avoided, as patient with benign biopsy results, concordant with imaging characteristics, need only follow-up [35]. Stereotactic 14-gauge automated biopsy avoids surgery in 76– 81% of lesions, resulting in a 40–58% decrease in the cost of diagnosis [36,37]. Liberman found that sonographically guided 14-gauge biopsy avoids surgery in 128 (85%) of 151 lesions and yields a 56% decrease in the cost of diagnosis [38]. The cost of managing probably benign lesions with surveillance mammography is eight times less expansive than CNB and the false negative rate is the same [39].
9.2. Reduction of the number of surgical procedures in breast cancer patients Because malignant FNA cannot make the diagnosis of invasive carcinoma and due to the risk of false positive cases associated with suspicious FNA, frozen section is still required before nodal dissection. Percutaneous biopsy replaces frozen section at the time of lumpectomy. In most centers frozen section is only performed for palpable lumps on surgical specimens, but cannot be done on excisional biopsy for microcalcifications. Malignant microcalcifications are due to ductal carcinoma in situ (50%), invasive carcinomas (25%) and ductal carcinomas with microinvasion (25%). Lymphadenectomy is not required for ductal carcinomas. On the other hand, the diagnosis of invasion is important to plan lymph node dissection, a one step surgery for treatment, instead of a two step surgery: one for diagnosis and one for treatment is possible. Sentinel lymph node biopsy with presurgical lymphoscintigraphy is increasing the need for a diagnosis of tumor invasion before surgery. Smith found that the average number of surgeries done was 1.25 in patients when the cancer was diagnosed by percutaneous biopsy prior to surgery versus 2.01 when cancer was diagnosed surgically [40]. In other studies, a single surgical procedure was performed in 84–90% of patients with percutaneously diagnosed cancer versus 24–29% for surgically diagnosed cancer [41–43].
10. Conclusion Mammographic screening results in positivity rates between 10 and 30%, 1–5% of which leads to further investigations; hence, nonsurgical diagnosis of nonpalpable lesions has been performed with different sampling techniques. We believe that masses are best targeted under ultrasound guidance and microcalcifications by stereotactic vacuum-assisted biopsy. FNA is a very cost-effective procedure, however, insufficient sampling rates and the impossibility to diagnose invasion are the main limits. Percutaneous biopsy is more time
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
consuming and expansive. Underestimation of DCIS and ADH is still possible, also less frequent with vacuum-assisted biopsy. Selection of patients and therapeutic consequence has to be worked-up. Currently these nonsurgical biopsy methods are most appropriately used in conjunction with radiologic and pathologic correlation and careful clinical management.
References [1] The uniform approach to breast fine needle aspiration biopsy. The final version. Breast J 1997;3(4):148 –68. [2] Azavedo E, Svane G, Auer G. Stereotactic fine needle biopsy in 2594 mammographically detected non-palpable lesions. Lancet 1989;1:1033 – 6. [3] Meunier M, Le Gal M, Klijanienko J, Vielh P, Neuenschwander S, Durand JC, Asselain B. Diagnostic des le´ sions mammaires non palpables: apport des ponctions cytologiques apre`s repe´ rage ste´ re´ otaxique. J Radiol 1995;76:259 –62. [4] Sneige N, Fornage BD, Saleh G. Ultrasound-guided fine-needle aspiration of non palpable breast lesions. Am J Clin Pathol 1994;102:98 – 101. [5] Thibault F, Meunier M, Klijanienko J, El Khoury C, Nos C, Vincent-Salomon A, Asselain B, Neuenschwander S. Diagnostic accuracy of sonography and combined sonographic assessment and sonographically guided cytology in nonpalpable solid breast lesions. J Clin Ultrasound 2000;28:387 – 98. [6] Verkooijen HM, Peeters PHM, Buskens E, Borel Rinkes IHM, Mali WPThM, Vroonhoven ThJMV. Diagnosis accuracy of large-core needle biopsy for nonpalpable breast disease: a metaanalysis. Br J Cancer 2000;82:1017 –21. [7] Sneige N. Specimen adequacy and false-negative diagnosis rate in FNA aspirates of palpable masses. Cancer 1998;84:344 – 8. [8] Sneige N. Fine needle-aspiration of the breast: a review of 1995 cases with emphasis on diagnostic pitfalls. Diagn Cytopathol 1993;9:106 – 12. [9] Mitnick JS, Vasquez MF, Feiner HD, Pressman P, Roses DF. The clinical significance of cytologic atypia in stereotactic fine needle aspiration biopsies of mammogram-detected breast lesions. Radiology 1996;198:319 –22. [10] Fajardo LI, Davis JR, Wiens JL, Trego DC. Mammographically-guided stereotactic fine needle aspiration cytology of nonpalpable breast lesions prospective comparison with surgical biopsy results. Am J Roentgenol 1990;198:319 – 22. [11] Mitnick JS, Vasquez MF, Feiner HD, Pressman P, Roses DF. The clinical significance of cytologic atypia in stereotactic fine needle aspiration biopsies of mammogram-detected breast lesions. Radiology 1996;198:319 –22. [12] Abendroth CS, Wang HH, Ducatman BS. Comparative features of carcinoma in situ and atypical ductal hyperplasia of the breast on fine needle aspiration biopsy specimens. Am J Clin Pathol 1991;96:654 – 9. [13] Thomas PA, Cangiarella J, Raab SS, Waisman J. Fine needle aspiration biopsy of proliferative breast disease. Mod Pathol 1995;8:130 – 6. [14] Sneige N, Staerkel GA. Fine needle aspiration cytology of ductal hyperplasia with and without atypia and ductal carcinoma in situ. Hum Pathol 1994;25:485 –92. [15] Sidawy MK, Stoler MH, Frable WJ, Frost AR, Massood S, Miller TR, Silverberg SG, Sneige N, Wang HH. Interobserver variability in the classification of proliferative breast lesions by fine-needle aspiration: results of the Papanicolaou Society of Cytopathology Study. Diagn Cytopathol 1998;18:150 – 65.
15
[16] Burbank F, Parker SH. Methods for evaluating the accuracy the quality of an image-guided breast biopsy program. Semin Breast Dis 1998;1:71 – 83. [17] Jackman R, Burbank F, Parker S, Evans W, Lechner MC, Richardson T, Smid A, Borofsky H, Lee C, Goldstein H, Schilling K, Wray A, Brem R, Helbich T, Lehrer D, Adler S. Stereotactic breast biopsy of nonpalpable lesions: determinants of ductal carcinoma in situ underestimation rates. Radiology 2001;218:497 – 502. [18] Darling ML, Smith DN, Lester SC, Kaelin C, Selland DL, Denison CM, Di Piro PJ, Rose DI, Rhei E, Meyer JE. Atypical ductal hyperplasia and ductal carcinoma in situ as revealed by large-core needle breast biopsy: results of surgical excision. Am J Roentgenol 2000;175:1341 – 6. [19] Philpotts LE, Lee CH, Horvath LJ, Lange RC, Carter D, Tocino I. Underestimation of breast cancer with 11-gauge vacuum suction biopsy. Am J Roentgenol 2000;175:1047 – 50. [20] Jacobs TW, Siziopikou KP, Prileau JE, Baum JK, Hayes DF, Schnitt SJ. Do pronostic marker studies on core needle biopsy specimens of breast carcinoma accurately reflect the marker status of the tumor? Mod Pathol 1998;11:259 – 64. [21] Sharifi S, Peterson MK, Baum JK, Raza S, Schnitt SJ. Assessment of pathologic prognostic factors in breast core needle biopsies. Mod Pathol 1999;12:941 – 5. [22] Homer MJ, Safaii H, Smith TJ, Marchant DJ. The relationship of mammographic microcalcification to malignancy: radiologic – pathologic correlation. Am J Roentgenol 1989;153:1187 –9. [23] Liberman L, Dershaw DD, Rosen PP, Morris EA, Abramson AF, Borgen PI. Percutaneous removal of malignant mammographic lesions at stereotactic vacuum-assisted biopsy. Radiology 1998;206:711 – 5. [24] Boppana S, May M, Hoda S. Does prior fine-needle aspiration cause diagnostic difficulties in histologic evaluation of breast carcinomas(abstract). Lab Invest 1994;70:13A. [25] Youngson BJ, Cranor M, Rosen PP. Epithelial displacement in surgical breast biopsies following needles procedures. Am J Surg Pathol 1994;18:896 – 903. [26] 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. [27] Diaz LK, Wiley EL, Venta LA. Are malignant cells displaced by large-gauge needle core biopsy of the breast? Am J Roentgenol 1999;173:1303 – 13. [28] Pisano E, Fajardo LL, Tsimikas J, Sneige N, Frable WJ, Gatsonis CA, Evans WP, Tocino I, Mc Neil BJ. Rate of insufficient samples for fine needle aspiration for nonpalpable breast lesions in a multicenter trial. Cancer 1998;82:679 – 88. [29] Pal S, Ikeda DM, Birdwell RL. Compliance with recommended follow-up after fine-needle aspiration biopsy of non palpable breast lesions: a retrospective study. Radiology 1996;201:71 – 4. [30] Parker SH, Burbank F, Jackman RJ, Aucreman CJ, Cardenosa G, Cink TM, Coscia JL, Eklund GW, Evans WP, Garver PR. Percutaneous large-core biopsy: a multi-institutional study. Radiology 1994;193:359 – 64. [31] Brenner RJ, Fajardo L, Fisher PR, Dershaw DD, Evans WP, Bassett L, Feig S, Mendelson E, Jackson V, Margolin FR. Percutaneous core biopsy of the breast: effect of operator experience and number of samples on diagnostic accuracy. Am J Roentgenol 1996;166:341 – 6. [32] March DE, Raslavicus A, Coughlin BF, Klein SV, Makari-Judson G. Use of breast core biopsy in the United States; results of a national survey. Am J Roentgenol 1997;169:697 – 701. [33] Liberman L, Abramson AF, Squires FB, Glassman JR, Morris EA, Dershaw DD. The breast Imaging Reporting and Data System: positive predictive value of mammographic features and final assessment categories. Am J Roentgenol 1998;171:35 –40.
16
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
[34] Cyrlak D. Induced costs of low-cost screening mammography. Radiology 1988;168:661 –3. [35] Ciatto S, Cecchini S, Grazzini G, Iosa A, Bartoli D, Cariaggi MP, Bulgaresi P. Positive predictive value of fine needle aspiration cytology of breast lesions. Acta Cytol 1989;33:894 – 8. [36] Liberman L, Fahs MC, Dershaw DD, Bonaccio E, Abramson AF, Cohen MA, Hann LE. Impact of stereotaxic core biopsy on cost of diagnosis. Radiology 1995;195:633 –7. [37] Lee CH, Egglin TIK, Philipotts LE, Maineniero MB, Tocino I. Cost effectiveness of stereotaxic biopsy for nonpalpable breast abnormalities: a decision analysis model. Acad Radiol 1996;3:351 – 60. [38] Liberman L, Feng TL, Dershaw DD, Morris EA, Abramson AF. Ultrasound-guided core breast biopsy: utility and cost-effectiveness. Radiology 1998;208:717 – 23. [39] Brenner RJ, Sickles EA. Surveillance mammography and
[40]
[41]
[42]
[43]
stereotactic core breast biopsy for probably benign lesions: a cost comparison analysis. Acad Radiol 1997;6:419 – 25. Smith DN, Christian R, Meyer JE. Large-core needle biopsy of nonpalpable breast cancers: the impact on subsequent surgical excision. Arch Surg 1997;132:256 – 9. Liberman L, LaTrenta LR, Dershaw DD, Abramson AF, Morris EA, Cohen AA, Rosen PP, Borgen PI. Impact of core biopsy on the surgical management of impalpable breast cancer. Am J Roentgenol 1997;168:495 – 9. Jackman RJ, Marzoni FA, Finkelstein SI, Shepard MJ. Benefits of diagnosing nonpalpable breast cancer with stereotactic large-core needle biopsy: lower costs and fewer operations(abst). Radiology 1996;201(P):311. Liberman L, Cody HS, Hill AD, Rosen PP, Yeh SD, Akhurst T, Morris EA, Abramson AF, Borgen PI, Dershaw DD. Sentinel lymph node biopsy after percutaneous diagnosis of nonpalpable breast cancer. Radiology 1999;211:835 – 44.
Fine needle aspiration cytology versus percutaneous biopsy of nonpalpable breast lesions M. Meunier a,*, K. Clough b a
Department of Radiology, Institut Curie, 26 rue d’Ulm, 75231 Paris Cedex 05, France Department of Surgery, Institut Curie, 26 rue d’Ulm, 75231 Paris Cedex 05, France
b
Received 27 November 2001; accepted 28 November 2001
Abstract Fine needle aspiration (FNA) and core biopsy (CB) are efficient alternatives to surgical biopsy: FNA provides a sampling of cells and is very cost effective. The main limits are insufficient sampling rate and the impossibility to diagnose invasion. CB allows architectural description and the diagnosis of specific benign and malignant lesions, but is more expensive and time-consuming. © 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Breast cancer; Fine needle aspiration; Percutaneous biopsy
1. Introduction In the last two decades, the diagnostic radiologist has gradually evolved from a passive interpreter of the mammogram to a physician who participates actively in the diagnosis of breast cancer. This evolution began with the expansion of fine needle aspiration (FNA) cytology under sonographic and stereotactic guidance. Percutaneous biopsies, primarily core biopsy (CB) developed later and were rapidly considered as an alternative to surgical biopsy. FNA provides a sampling of cells (cytological material). Percutaneous biopsies yield a large core of tissue in which the architectural description and tissue elements recognition is possible (histology material) with the diagnoses of specific benign and malignant lesions. These interventional procedures reduce the number of unnecessary excisional biopsies for benign lesions and lower the false positive cases and cost of screening. CB replaces frozen section during lumpectomy. Axillary dissection in most institutions is performed only for invasive carcinomas. In doing so, cancer surgery will * Corresponding author. Tel.: +33-1-4432-4200; fax: + 33-1-44324015. E-mail address: [email protected] (M. Meunier).
necessitate only a one step surgery for treatment, instead of a two step surgery: one for diagnosis and one for treatment.
1.1. Objecti6e To compare, contrast and analyze the value and limitations of FNA and percutaneous biopsies.
2. Techniques
2.1. Fine needle aspiration cytology FNA is performed with a 20–23 gauge needle, which is often attached to a syringe. Once the needle is introduced into the lesion, negative pressure is applied by pulling back on the syringe, allowing the aspiration of material for sampling. Numerous multidirectional passes through the lesion increase the probability of successful sampling, especially in small lesions. The cellular material is preserved on slides for interpretation by the cytopathologist. FNA is accomplished in a relatively short period of time. Sampling of different lesions is easily feasible.
0720-048X/02/$ - see front matter © 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 7 2 0 - 0 4 8 X ( 0 1 ) 0 0 4 8 0 - 6
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
2.2. Percutaneous biopsy CB is performed with a specially designed 14–18 gauge needle that is placed in an automated biopsy gun. Once the needle is positioned at the appropriate depth, the spring loaded gun rapidly advances into the lesion, taking a core of tissue during its excursion. At least four or five passes through the lesion are needed. CB allows a monodirectional sampling of the target. This inconvenience is compensated by aspiration with the vacuum assisted device, which allows harvesting of larger quantity of tissue with a single needle insertion. After targeting, while the suction is on, specimens are obtained by rotating the aperture of the bowl clockwise with 2 h increments. Roughly 1 cm3 of tissue is removed when 12 specimens are done per tour. Both are performed under stereotactic or sonographic guidance. Depending on the modality of guidance used, a percutaneous biopsy requires 30 min to 1 h to perform. Histological samples are preserved in formalin for interpretation by a histopathologist.
3. Results There is no strict criteria for reporting cytologic results. FNA can be reported as malignant, suspicious for carcinoma, benign or insufficient specimen. A standardized uniform terminology into five categories (unsatisfactory, benign, indeterminate/atypical, suspicious/probably malignant and malignant) has been recommended by The National Cancer Institute [1]. FNA cannot make the diagnosis of invasive carcinoma; in most institutions frozen section at the time of lumpectomy is still required before planning lymph node dissection. Advantages of percutaneous biopsy over FNA are: the accurate diagnosis of specific benign and malignant lesions; the recognition of a specific benign lesion and differ-
11
entiation between true negative specific benign lesion and false negative result due to sampling error; the differentiation between invasive and noninvasive cancers; tumor grading.
3.1. Fine needle aspiration cytology Data from published series are difficult to compare because study designs, techniques and cases selection differ significantly. There are no strict criteria for classification of atypia or suspicious lesions. Surgical biopsy is recommended for suspicious lesions because a nonnegligible percentage will turn out to be malignant. Table 1 presents the results of FNA with surgical correlation.
3.2. Percutaneous biopsy Numerous studies and a recent meta-analysis were published [6]. Preset inclusion criteria were: nonpalpable lesion; all histological diagnoses of CB specimens had to be confirmed by either surgical biopsy or 2 years follow-up; the absolute number of benign and malignant diagnoses had to be derivable; a minimum of at least five cores had to be obtained. A total of 865 CB were done, the overall sensitivity was 97%, 3% false negative, the malignancy rate varies between 23 and 57%. Despite benign CB results, authors insist upon the impact of breast cancer prevalence of the lesions detected by screening and referred for biopsy. In a population: with a low prevalence of malignancy e.g. 20%, the probability of cancer being present despite benign CB is low: 0.6%. with a prevalence of 50% the probability of carcinoma being present will still be 3%.
Table 1 Results of FNA with sugical correlation Authors
Guidance
Total (ratio B/M)
NS
True negative
True positive
False negative
False positive
Azavedo et al. [2]
Stereotactic
567 (138/429)
49 27 cancers
102 (20%)
285 (55%)
117 (22%)
14 (3%)
Meunier et al. [3]
Stereotactic
228 (103/125)
59 34 cancers
74 (44%)
86 (51%)
7 (4%)
4 (2%)
Sneige et al. [4]
Ultrasound
254 (83/168)
27 12 cancers
65 (29%)
152 (67%)
4 (2%)
4 (2%)
Thibault et al. [5]
Ultrasound
174 (79/95)
14 6 cancers
66 (41%)
80 (50%)
9 (6%)
5 (3%)
12
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
4. Diagnosis accuracy
4.1. FNA The false negative cases are attributed to sampling errors, specimen quality or to characteristics of the lesion: infiltrating lobular carcinoma or marked desmoplasia. In a series from 4455 FNA of palpable masses, 41 false negative aspirations were reviewed. No interpretation errors were identified. Twenty-one FNA (51%) were classified as adequate (8– 100 well preserved cells) and 20 FNA (48%) as inadequate (less than six cells). Cases of invasive lobular carcinoma were more common in the false-negative smears with inadequate sampling [7]. FNA in experienced hands, has a reported false positive rate around 2%, very close to frozen section examination. After conservative treatment, radiationinduced changes can be interpreted as recurrent carcinoma. Of the 49 suspicious tumors reported by Sneige 38 (76%) were found to be malignant. Eleven (22.4%) were benign after excisional biopsy: two mucocelelike lesions, one nipple adenoma, one adenosis, three ductal hyperplasia and three fibroadenomas [8]. Apocrine cysts with alarming cytologic atypia can be misinterpreted as carcinoma. Proliferative breast disease includes hyperplasia without atypia, hyperplasia with atypia and carcinoma in situ. The diagnosis of these lesions is important in identifying women at an increased risk for breast cancer: the risk is 1.5 to 2-fold for proliferative lesions without atypia, 4 to 5-fold with proliferative lesions with atypia and 8 to 10-fold with carcinoma in situ. With the increased use of FNA, cytopathologists are often asked to differentiate such entities and depending on the threshold chosen the rate varies from 2 to 22% [9,10]. Cytologic findings of atypia in FNA samples should prompt excisions, 61% of these cases proved malignant [11]. Cytopathologists have tried to establish different criteria [12,13] and insist on architectural features [14]. Interobserver variability in classification of proliferative breast lesions has been reported, exact cytohistologic correlation being achieved in only 36% of cases [15].
4.2. Percutaneous biopsy Burbank and Parker introduced a method to evaluate the accuracy and the quality of an image-guided breast biopsy program [16]. The histologic diagnoses of CB and surgical specimens are classified in four categories: benign disease; high risk lesions: atypical ductal hyperplasia, lobular carcinoma in situ, atypical lobular hyperplasia and radial scar; ductal carcinoma in situ; infiltrating carcinoma.
The miss rate is the percentage of all cancers diagnosed as benign by CB; it is estimated around 3%. A lesion is concordant when pathology is the same for CB and lumpectomy. Benign lesions are followed and if stable are classified as benign. A lesion is overestimated when upgraded by CB. A lesion is underestimated when a lower degree of pathology is described at CB than at lumpectomy. This group is divided in two categories: the DCIS underestimated rate defined as the percentage of DCIS on CB upgraded in invasive carcinoma on lumpectomy; the ADH underestimated rate, defined as the percentage of ADH on CB that is upgraded to DCIS or invasive. ADH are classified with underestimated lesions and not as false negative cases, because open surgery is recommended, specially if all the target had been removed. For percutaneous biopsy, underestimation seems related to the effect of biopsy device, to probe size, mammographic lesion type, lesion size and number of samples.
4.2.1. CB may fail to show in6asi6e carcinoma In a multicentric study, the rate of underestimation of DCIS was 20.4% for lesions diagnosed at CB and 11.2% of lesions diagnosed at vacuum-assisted biopsy. DCIS underestimation was 1.9 times more frequent with masses than with calcifications, 1.8 times more frequent with CB than with vacuum-assisted biopsy, and 1.5 times more frequent with ten or fewer specimens per lesion than with more than ten specimens per lesion [17]. 4.2.2. CB may fail to show DCIS For lesions diagnosed initially as atypical ductal hyperplasia, underestimation of DCIS and invasive ductal carcinoma was significantly less frequent using the 11gauge directional vacuum-assisted device compared with the 14-gauge directional vacuum-assisted device (19 vs. 39%, P= 0.025) and with the automated 14gauge needle (19 vs. 44%, P= 0,01) [18]. Finally, the underestimation rate for calcifications was 16.3% (14/ 86) and 1.6% (1/64) for masses. No underestimation was found if the entire lesion was removed at vacuum suction biopsy [19]. Lobular carcinoma in situ (LCIS) is an incidental finding, occult mammographically. When the pathologic results shows only LCIS, surgical excision is usually recommended because the mammographic target may be missed and breast cancer is often associated with LCIS nearby. Benign or malignant papillary lesions are accurately diagnosed with CB in the majority of the cases, but cases diagnosed as suspicious for malignancy or with atypia or unusual associated histologic findings should be excised.
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
Radial scars often appear as areas of architectural distortion and are frequently associated with carcinoma. Carcinoma is more frequent when the size of the radial scar is more than 5 mm or patients older than 40 years. It has generally been advised that radial scar should be excised surgically; when diagnosed at CB surgery is still recommended.
5. Prognostic factors FNA and CB are being used increasingly as the initial diagnostic procedure. Clinicians are interested in obtaining as much prognostic information as possible from these limited specimens. FNA material can be evaluated for specific biochemical molecular markers including steroid hormone receptor status, flow cytometry to determine DNA content (ploidy) and the percentage of cells that are in the growth portion of the cell cycle (S-phase fraction). CB specimens allow immunohistochemical assessment of estrogen and progesterone receptor status, c-erbB-2 and p53 [20]. Tumor cellularity is evaluated by counting cells within one high power field. For invasive carcinomas, tumor size, histologic grade, lymphatic invasion, and extensive intraductal carcinomas are important prognostic factors. Histologic grade between CB and surgical specimens are discordant in 25% of cases. Inversely the evaluation of tumor size, lymphatic vessel invasion and intraductal component is severely limited in CB specimens [21].
13
the lesion; but vacuum-assisted biopsy can remove a small target. The goal of percutaneous breast biopsy is diagnosis, not treatment. Complete removal of a target does not ensure complete excision of the histologic abnormalities. Residual carcinoma was found in 75% of 15 carcinomas in which the target was removed by 11-gauge vacuum-assisted biopsy [23]. The rational for removal of most the mammographic abnormality is to compensate for sampling error and underestimation. After total excision of microcalcifications, a radioopaque clips should be left in place because histology can turn out to be malignant and preoperative needle localization impossible. Furthermore, a complete removal of a target might decrease the anxiety of patients and in young patients would have a consequence on the rhythm of follow-up.
6.3. Needle track seeding The displacement of malignant cells away from the target has been described with FNA, CB or wire localization [24–26]. There is no evidence that the displaced epithelium is viable, however, it can lead to histologic interpretation errors: displaced DCIS can mimic infiltrating ductal carcinoma. The frequency of epithelial displacement after 14-gauge CB is reported to be higher than after directional vacuum-assisted biopsy [27]. Longterm follow-up of cancers diagnosed by percutaneous biopsy is necessary to determine the significance of needle track seeding on local recurrence and survival.
6.4. Insufficient specimens rate 6. Limits and controversies
6.1. Targeting When seen sonographically, masses are best reached under ultrasound guidance. Fine needle position or pre-fire and post-fire needle should be shown on films. Under stereotactic guidance good lesions conspicuity on stereotactic pairs of images obtained before and during the procedure and needle positions on the pre-fire and post fire position should be documented. Architectural distortions are very difficult to target because they change on pair images. The target can be displaced or masked by hemorrhage or xylocain. For microcalcifications, specimen radiography is needed to confirm the quality of sampling. The resolution of current digital systems is still inferior to that on screen-film techniques: as a result, subtle microcalcifications can be difficult to target. Finally, in 16% of cases, cancers are found near but at a distance from the targeted microcalcifications [22].
6.2. Complete excision 6ersus sampling With FNA and CB, diagnosis is made by sampling of
For nonpalpable breast lesions, the insufficient samples rate of FNA varies between studies. In a multicentric trial, the overall insufficient sampling rates were 40% for stereotactic guidance and 8.45% for ultrasound guidance [28]. This difference can be partly explained by the modality of sampling: multidirectional by ultrasound guidance and monodirectional with stereotactic guidance. FNA that yields insufficient specimens add to the costs of screening because patients usually have to go onto excisional biopsy. The most effective way to reduce insufficient specimen rates is to have a cytopathologist who can immediately stain and microscopically evaluate the smears, additional aspirations being performed immediately when necessary. In contrast to FNA, CB produces few insufficient samples.
7. Follow-up Cytologic diagnoses must be correlated with the clinical and imaging findings (the triple test) to reduce the rate of false-negative cases, but concordant benign triple tests do not entirely exclude the possibility of
14
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
carcinoma, and such cases require periodic follow-up. Noncompliance of half of the patients with follow-up recommendations is an important issue undermining the benefits of FNA [29]. Because CB is a sampling rather than an excisional technique, the issue of patient follow– up after the procedure has been raised. Parker proposes follow–up mammography at 6 months for benign biopsy results concordant with the imaging findings and annual screening if no significant change is evident [30]. Brenner proposes follow-up mammograms at 6, 12, 24 and 36 months [31]. The appropriate interval and duration of follow-up in different situations needs further assessment and clarification. Compliance of patients to follow-up remains an important concern. In a national survey the reported time for follow-up was 12 months [32].
8. Multidisciplinary approach Close collaboration of a multidisciplinary team is necessary in managing patients after image guided breast biopsy procedures. Radiologists should consider what histologic diagnoses they will accept for every abnormalities biopsied. When pathologic results are congruent with the radiologic abnormalities, follow-up is proposed. If pathologic results show no evidence of malignant tumor but the radiologic lesion is highly suspicious, after review of needle position and samples, preoperative needle localization is recommended.
9. Socio-economic outcome
9.1. Lower the cost of screening Screening mammography is believed to reduce breast carcinoma mortality for women aged over 50 years. Since mammographic findings are nonspecific, and although in most cases it is possible to differentiate between benign and malignant abnormalities, large numbers of breast biopsies for benign lesions are generated. It has been estimated that 11– 30% of screening mammography disclose nonpalpable lesions, 1– 5% lead to a biopsy and 0.5% of abnormalities will reveal a cancer [33]. The positive biopsies vary between 30 and 60% in Europe and 10 and 30% in the USA. Approximately 32% of the total cost of breast carcinoma screening is due to open surgical biopsy for benign lesions [34]. FNA cytology and percutaneous biopsy are noninvasive, cost effective procedures. They allow a rapid determination of the nature of equivocal lesions and relief of anxiety of patient, eliminating 4– 6 months followup. For many women with benign breast disease,
surgery is avoided, as patient with benign biopsy results, concordant with imaging characteristics, need only follow-up [35]. Stereotactic 14-gauge automated biopsy avoids surgery in 76– 81% of lesions, resulting in a 40–58% decrease in the cost of diagnosis [36,37]. Liberman found that sonographically guided 14-gauge biopsy avoids surgery in 128 (85%) of 151 lesions and yields a 56% decrease in the cost of diagnosis [38]. The cost of managing probably benign lesions with surveillance mammography is eight times less expansive than CNB and the false negative rate is the same [39].
9.2. Reduction of the number of surgical procedures in breast cancer patients Because malignant FNA cannot make the diagnosis of invasive carcinoma and due to the risk of false positive cases associated with suspicious FNA, frozen section is still required before nodal dissection. Percutaneous biopsy replaces frozen section at the time of lumpectomy. In most centers frozen section is only performed for palpable lumps on surgical specimens, but cannot be done on excisional biopsy for microcalcifications. Malignant microcalcifications are due to ductal carcinoma in situ (50%), invasive carcinomas (25%) and ductal carcinomas with microinvasion (25%). Lymphadenectomy is not required for ductal carcinomas. On the other hand, the diagnosis of invasion is important to plan lymph node dissection, a one step surgery for treatment, instead of a two step surgery: one for diagnosis and one for treatment is possible. Sentinel lymph node biopsy with presurgical lymphoscintigraphy is increasing the need for a diagnosis of tumor invasion before surgery. Smith found that the average number of surgeries done was 1.25 in patients when the cancer was diagnosed by percutaneous biopsy prior to surgery versus 2.01 when cancer was diagnosed surgically [40]. In other studies, a single surgical procedure was performed in 84–90% of patients with percutaneously diagnosed cancer versus 24–29% for surgically diagnosed cancer [41–43].
10. Conclusion Mammographic screening results in positivity rates between 10 and 30%, 1–5% of which leads to further investigations; hence, nonsurgical diagnosis of nonpalpable lesions has been performed with different sampling techniques. We believe that masses are best targeted under ultrasound guidance and microcalcifications by stereotactic vacuum-assisted biopsy. FNA is a very cost-effective procedure, however, insufficient sampling rates and the impossibility to diagnose invasion are the main limits. Percutaneous biopsy is more time
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
consuming and expansive. Underestimation of DCIS and ADH is still possible, also less frequent with vacuum-assisted biopsy. Selection of patients and therapeutic consequence has to be worked-up. Currently these nonsurgical biopsy methods are most appropriately used in conjunction with radiologic and pathologic correlation and careful clinical management.
References [1] The uniform approach to breast fine needle aspiration biopsy. The final version. Breast J 1997;3(4):148 –68. [2] Azavedo E, Svane G, Auer G. Stereotactic fine needle biopsy in 2594 mammographically detected non-palpable lesions. Lancet 1989;1:1033 – 6. [3] Meunier M, Le Gal M, Klijanienko J, Vielh P, Neuenschwander S, Durand JC, Asselain B. Diagnostic des le´ sions mammaires non palpables: apport des ponctions cytologiques apre`s repe´ rage ste´ re´ otaxique. J Radiol 1995;76:259 –62. [4] Sneige N, Fornage BD, Saleh G. Ultrasound-guided fine-needle aspiration of non palpable breast lesions. Am J Clin Pathol 1994;102:98 – 101. [5] Thibault F, Meunier M, Klijanienko J, El Khoury C, Nos C, Vincent-Salomon A, Asselain B, Neuenschwander S. Diagnostic accuracy of sonography and combined sonographic assessment and sonographically guided cytology in nonpalpable solid breast lesions. J Clin Ultrasound 2000;28:387 – 98. [6] Verkooijen HM, Peeters PHM, Buskens E, Borel Rinkes IHM, Mali WPThM, Vroonhoven ThJMV. Diagnosis accuracy of large-core needle biopsy for nonpalpable breast disease: a metaanalysis. Br J Cancer 2000;82:1017 –21. [7] Sneige N. Specimen adequacy and false-negative diagnosis rate in FNA aspirates of palpable masses. Cancer 1998;84:344 – 8. [8] Sneige N. Fine needle-aspiration of the breast: a review of 1995 cases with emphasis on diagnostic pitfalls. Diagn Cytopathol 1993;9:106 – 12. [9] Mitnick JS, Vasquez MF, Feiner HD, Pressman P, Roses DF. The clinical significance of cytologic atypia in stereotactic fine needle aspiration biopsies of mammogram-detected breast lesions. Radiology 1996;198:319 –22. [10] Fajardo LI, Davis JR, Wiens JL, Trego DC. Mammographically-guided stereotactic fine needle aspiration cytology of nonpalpable breast lesions prospective comparison with surgical biopsy results. Am J Roentgenol 1990;198:319 – 22. [11] Mitnick JS, Vasquez MF, Feiner HD, Pressman P, Roses DF. The clinical significance of cytologic atypia in stereotactic fine needle aspiration biopsies of mammogram-detected breast lesions. Radiology 1996;198:319 –22. [12] Abendroth CS, Wang HH, Ducatman BS. Comparative features of carcinoma in situ and atypical ductal hyperplasia of the breast on fine needle aspiration biopsy specimens. Am J Clin Pathol 1991;96:654 – 9. [13] Thomas PA, Cangiarella J, Raab SS, Waisman J. Fine needle aspiration biopsy of proliferative breast disease. Mod Pathol 1995;8:130 – 6. [14] Sneige N, Staerkel GA. Fine needle aspiration cytology of ductal hyperplasia with and without atypia and ductal carcinoma in situ. Hum Pathol 1994;25:485 –92. [15] Sidawy MK, Stoler MH, Frable WJ, Frost AR, Massood S, Miller TR, Silverberg SG, Sneige N, Wang HH. Interobserver variability in the classification of proliferative breast lesions by fine-needle aspiration: results of the Papanicolaou Society of Cytopathology Study. Diagn Cytopathol 1998;18:150 – 65.
15
[16] Burbank F, Parker SH. Methods for evaluating the accuracy the quality of an image-guided breast biopsy program. Semin Breast Dis 1998;1:71 – 83. [17] Jackman R, Burbank F, Parker S, Evans W, Lechner MC, Richardson T, Smid A, Borofsky H, Lee C, Goldstein H, Schilling K, Wray A, Brem R, Helbich T, Lehrer D, Adler S. Stereotactic breast biopsy of nonpalpable lesions: determinants of ductal carcinoma in situ underestimation rates. Radiology 2001;218:497 – 502. [18] Darling ML, Smith DN, Lester SC, Kaelin C, Selland DL, Denison CM, Di Piro PJ, Rose DI, Rhei E, Meyer JE. Atypical ductal hyperplasia and ductal carcinoma in situ as revealed by large-core needle breast biopsy: results of surgical excision. Am J Roentgenol 2000;175:1341 – 6. [19] Philpotts LE, Lee CH, Horvath LJ, Lange RC, Carter D, Tocino I. Underestimation of breast cancer with 11-gauge vacuum suction biopsy. Am J Roentgenol 2000;175:1047 – 50. [20] Jacobs TW, Siziopikou KP, Prileau JE, Baum JK, Hayes DF, Schnitt SJ. Do pronostic marker studies on core needle biopsy specimens of breast carcinoma accurately reflect the marker status of the tumor? Mod Pathol 1998;11:259 – 64. [21] Sharifi S, Peterson MK, Baum JK, Raza S, Schnitt SJ. Assessment of pathologic prognostic factors in breast core needle biopsies. Mod Pathol 1999;12:941 – 5. [22] Homer MJ, Safaii H, Smith TJ, Marchant DJ. The relationship of mammographic microcalcification to malignancy: radiologic – pathologic correlation. Am J Roentgenol 1989;153:1187 –9. [23] Liberman L, Dershaw DD, Rosen PP, Morris EA, Abramson AF, Borgen PI. Percutaneous removal of malignant mammographic lesions at stereotactic vacuum-assisted biopsy. Radiology 1998;206:711 – 5. [24] Boppana S, May M, Hoda S. Does prior fine-needle aspiration cause diagnostic difficulties in histologic evaluation of breast carcinomas(abstract). Lab Invest 1994;70:13A. [25] Youngson BJ, Cranor M, Rosen PP. Epithelial displacement in surgical breast biopsies following needles procedures. Am J Surg Pathol 1994;18:896 – 903. [26] 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. [27] Diaz LK, Wiley EL, Venta LA. Are malignant cells displaced by large-gauge needle core biopsy of the breast? Am J Roentgenol 1999;173:1303 – 13. [28] Pisano E, Fajardo LL, Tsimikas J, Sneige N, Frable WJ, Gatsonis CA, Evans WP, Tocino I, Mc Neil BJ. Rate of insufficient samples for fine needle aspiration for nonpalpable breast lesions in a multicenter trial. Cancer 1998;82:679 – 88. [29] Pal S, Ikeda DM, Birdwell RL. Compliance with recommended follow-up after fine-needle aspiration biopsy of non palpable breast lesions: a retrospective study. Radiology 1996;201:71 – 4. [30] Parker SH, Burbank F, Jackman RJ, Aucreman CJ, Cardenosa G, Cink TM, Coscia JL, Eklund GW, Evans WP, Garver PR. Percutaneous large-core biopsy: a multi-institutional study. Radiology 1994;193:359 – 64. [31] Brenner RJ, Fajardo L, Fisher PR, Dershaw DD, Evans WP, Bassett L, Feig S, Mendelson E, Jackson V, Margolin FR. Percutaneous core biopsy of the breast: effect of operator experience and number of samples on diagnostic accuracy. Am J Roentgenol 1996;166:341 – 6. [32] March DE, Raslavicus A, Coughlin BF, Klein SV, Makari-Judson G. Use of breast core biopsy in the United States; results of a national survey. Am J Roentgenol 1997;169:697 – 701. [33] Liberman L, Abramson AF, Squires FB, Glassman JR, Morris EA, Dershaw DD. The breast Imaging Reporting and Data System: positive predictive value of mammographic features and final assessment categories. Am J Roentgenol 1998;171:35 –40.
16
M. Meunier, K. Clough / European Journal of Radiology 42 (2002) 10–16
[34] Cyrlak D. Induced costs of low-cost screening mammography. Radiology 1988;168:661 –3. [35] Ciatto S, Cecchini S, Grazzini G, Iosa A, Bartoli D, Cariaggi MP, Bulgaresi P. Positive predictive value of fine needle aspiration cytology of breast lesions. Acta Cytol 1989;33:894 – 8. [36] Liberman L, Fahs MC, Dershaw DD, Bonaccio E, Abramson AF, Cohen MA, Hann LE. Impact of stereotaxic core biopsy on cost of diagnosis. Radiology 1995;195:633 –7. [37] Lee CH, Egglin TIK, Philipotts LE, Maineniero MB, Tocino I. Cost effectiveness of stereotaxic biopsy for nonpalpable breast abnormalities: a decision analysis model. Acad Radiol 1996;3:351 – 60. [38] Liberman L, Feng TL, Dershaw DD, Morris EA, Abramson AF. Ultrasound-guided core breast biopsy: utility and cost-effectiveness. Radiology 1998;208:717 – 23. [39] Brenner RJ, Sickles EA. Surveillance mammography and
[40]
[41]
[42]
[43]
stereotactic core breast biopsy for probably benign lesions: a cost comparison analysis. Acad Radiol 1997;6:419 – 25. Smith DN, Christian R, Meyer JE. Large-core needle biopsy of nonpalpable breast cancers: the impact on subsequent surgical excision. Arch Surg 1997;132:256 – 9. Liberman L, LaTrenta LR, Dershaw DD, Abramson AF, Morris EA, Cohen AA, Rosen PP, Borgen PI. Impact of core biopsy on the surgical management of impalpable breast cancer. Am J Roentgenol 1997;168:495 – 9. Jackman RJ, Marzoni FA, Finkelstein SI, Shepard MJ. Benefits of diagnosing nonpalpable breast cancer with stereotactic large-core needle biopsy: lower costs and fewer operations(abst). Radiology 1996;201(P):311. Liberman L, Cody HS, Hill AD, Rosen PP, Yeh SD, Akhurst T, Morris EA, Abramson AF, Borgen PI, Dershaw DD. Sentinel lymph node biopsy after percutaneous diagnosis of nonpalpable breast cancer. Radiology 1999;211:835 – 44.