Needle Aspiration Biopsy of Palpable Breast Masses Michael P. Kahky, Mo, V. Rene Rone, MD, Diane L. Duncan, CT(ASCP), Anatolio B. Cruz, Jr., Mo, Harold V. Gaskill III, MD, San Antonio, Texas One hundred fifteen patients underwent needle aspiration biopsy of palpable breast masses prior to open biopsy. Aspirates were obtained by surgical residents, prepared by a eytotechnologist present at the procedure, and evaluated by a single pathologist. Cytologic findings were interpreted as positive or highly suspicious for malignancy, normal or benign, or insufficient. All patients underwent open biopsy. Patients with positive or highly suspicious cytologic findings who preferred partial mastectomy and radiotherapy were offered a segmental mastectomy. No patient was offered total mastectomy based on cytologic findings alone. There were two false-positive and two false-negative results, for a 92 percent sensitivity and 97 percent specificity. The value of needle aspiration biopsy lies in its ability to identify patients at high risk for malignancy. Total mastectomy cannot be recommended based on cytologic findings alone. The setting of a surgical residency program does not adversely affect the reliability of the technique.
N
eedle aspiration biopsy has become a valuable adjunct to the evaluation of palpable breast masses. Growing public awareness of the problem of breast cancer and of the therapeutic alternatives to radical mastectomy have rendered the one-stage biopsy and mastectomy procedure obsolete. Patients need ample time after the diagnosis of malignancy to consult with family and other physicians regarding the optimal form of definitive therapy. Needle aspiration biopsy enables the clinician to identify patients with a strong likelihood of malignancy at the time of initial evaluation. Aspiration can be done quickly with a low risk of complication, and patient acceptance is excellent. Recent reports confirm the accuracy and reliability of the technique, and some centers use a cytologic diagnosis of malignancy as the major indicator for definitive therapy [1-6]. Since needle aspiration biopsy of breast masses has been routinely performed at our institution, we reviewed From the Department of Surgery, University of Texas Health Science Center, San Antonio, Texas. Requests for reprints should be addressed to Harold V. Gaskill III, MD, Department of Surgery, 7703 Hoyd Curl Drive, San Antonio, Texas 78284-7842. Presented at the 40th Annual Meeting of the Southwestern Surgical Congress, Phoenix, Arizona, April 10-13, 1988.
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the experience from August 1986 through August 1987 to assess its prognostic value as well as its impact on patient management. MATERIAL AND METHODS All patients being evaluated for a palpable breast mass at the University of Texas Medical Center Hospital underwent fine-needle aspiration biopsy prior to open biopsy. During the study period, a total of 115 patients were evaluated, including 3 male patients. Their ages ranged from 12 to 69 years (mean 39 years). Aspiration was performed by surgical residents at all levels of training. After obtaining written informed consent, the skin overlying the mass was prepared with povidone-iodine soaked pledgets. Aspiration was performed using a 22-gauge needle and 20-ml syringe using multiple passes and continuous suction. The aspirated material was smeared immediately on nonfrosted slides, fixed in 95 percent methanol solution, and stained by a modified Papanicolau method. All specimens were prepared by a cytotechnologist present at the procedure and evaluated the same day by a single pathologist with special expertise in breast cytology. Interpretation was divided into the following categories: (1) positive for malignancy; (2) highly suspicious for malignancy; (3) normal or benign disease; (4) insufficient material for diagnosis. All patients had open biopsy for histologic confirmation. Positive or highly suspicious cytologic findings facilitated an early discussion of definitive treatment with the patient. Patients preferring partial mastectomy and radiotherapy were offered a segmental mastectomy or big biopsy for lesions interpreted as positive or highly suspicious for malignancy. Patients who chose modified radical mastectomy had an open biopsy first. No patient was offered total mastectomy based on cytologic findings alone. Patients with benign findings or an unsatisfactory specimen underwent biopsy through a circumareolar incision. RESULTS Needle aspiration cytology was performed in 115 patients; of these, 15 (13 percent) had findings positive for cancer, 9 (8 percent) had highly suspicious findings, and 12 (10 percent) had insufficient material for diagnosis. The specimen was negative for cancer in 79 patients (69 percent). Twenty-four patients proved to have malignancy on open biopsy. The majority of the malignancies in this series (75 percent) were infiltrating ductal carcinomas. Four patients (17 percent) had infiltrating lobular carcinoma, and one patient (4 percent) had invasive comedocarcinoma. One patient with lymphoma of the breast was correctly diagnosed by cytologic assessment. Cytologic findings correlated with open biopsy findings as shown in Table I. There were two false-positive and two false-
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TABLE I
Findings on Needle Aspiration and Open Biopsy Cytologic Findings Positive
Histologic Findings Benign Malignant 1
14
1
8
77
2
12
0
(n = 15)
Highly suspicious
(/)
,~
Mar~nant
22
20-
#.
9
10-
m|o
(n = 9)
Benign (n = 79)
Insufficient material for diagnosis (n = 12)
10-19
F i g u r e 1.
negative results. These results yielded a sensitivity of 92 percent, a specificity of 97 percent, and a predictive value of 92 percent. The distribution of all lesions and the percentage of malignant lesions per age group are shown in Figure 1. The proportion of patients with malignant lesions increased with increasing age. Although patients older than 50 years of age accounted for only 25 percent of the total number of patients, 71 percent of the patients with malignancy were older than 50 years of age. The mean age of patients with malignant lesions was 55.25 4. 10.29 years (mean 4- SD), and for patients with benign lesions, 35.13 4. 12.85 years. The difference between these values was significant (SE = 8.064, p <0.001). Both false-positive results in our series occurred in patients with subareolar masses. The first patient presented with a 1.5 cm mass which was thought to be gritty on aspiration. Cytologic findings were interpreted as being consistent with adenocarcinoma and included features suggestive of intraductal papillomatosis. A segmental m a s t e e t o m y was performed, and pathologic examination of the operative specimen revealed intraductal papillomatosis with no evidence of malignancy. The second patient presented with a hard, 2.5 cm subareolar nodule. Aspiration cytologic findings were interpreted as suspicious for carcinoma. Open biopsy, however, revealed a fibroadenoma. There were two false-negative results. The first patient presented with a 3 by 4 cm mass which had been present for 3 years. Findings on cytologic examination were consistent with chronic mastitis, fat necrosis, or both. Open biopsy revealed infiltrating lobular carcinoma. The second patient presented with a 1.5 by 1.5 cm mass which was suspicious for malignancy both on mammogram and sonogram. Although the cytologic findings were suggestive of fibroadenoma, open biopsy revealed infiltrating ductal carcinoma. COMMENTS Needle aspiration biopsy has been widely used in the diagnosis of solid masses since its introduction in the United States in 1930 by Morton and Ellis [7]; however, it has only recently been applied to the diagnosis of breast masses. Recent reports have demonstrated that needle asp!ration biopsy is a rapid and reliable method of establishing a diagnosis in the majority of patients with palpa-
20-29
30~39 40~49 Age
50~59
60~69
Distribution of lesions according to patient age.
ble breast masses [I-6]. The advantages ofthe technique include excellent patient acceptance, low incidence of complications, and minimal expense. Needle aspiration biopsy enables the clinician to identify p~ttients at high risk for malignancy and allows for early discussion and planning of definitive therapy. A cytopathologist with a special interest in breast cytology is essential if the test is to be clinically useful. Similarly, familiarity of the physician with aspirating solid masses is also considered a key factor. Large series often describe only one or two physicians performing the procedure. Barrows [4] recently reviewed his experience with needle aspiration of breast masses and found that the rate of positive specimens increased proportionately with the skill of the physician performing the biopsy. The proficiency of the individual perfoi'ming the procedure and the size of the lesion were the two most significant variables in determining the accuracy of the technique in Barrows' series. In general, the rate of inadequate or acellular specimens is indicative of the experience of the aspirator. In our series, all aspirates were performed by surgical house staff. The specificity and sensitivity rates were comparable to those reported in other large series, and the rate of inadequate specimens was 10 percent, again comparable to other large series. Therefore, we do not believe that involvement of surgical house staff adversely affected the reliability of the technique. A positive finding on cytologic needle biopsy is the major indicator for mastectomy in some centers [5,6]. A high degree of confidence in and rapport with the cytopathologist is stressed. In addition, the criteria for a positive cytologic diagnosis are strict, and any specimens that do not fulfill the criteria are defined as suspicious, with recommendations for open biopsy. Both false-positive resuits in our series occurred toward the end of the study period, when both surgeon and pathologist felt comfortable with the procedure. Currently, because there is a risk of false-positive results, our policy is to perform open biopsy prior to total mastectomy. However, if a patient selects partial mastectomy and radiation, we proceed with operation on the basis of positive or highly suspicious cytologic findings. The predictive value of negative cytologic findings
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must be taken in the context of the clinical setting. Most investigators agree that a negative finding does not exclude malignancy reliably and is an indication for open biopsy. Both false-negative results in our series were in women with masses that were either clinically suspicious or suspicious on mammography. Goodson [8] followed 204 patients with benign findings on needle aspiration 3 years after diagnosis and found cancer in 6. He emphasized that a benign finding, taken in context, is a reasonable contraindication to open biopsy but should not be used as a basis for ignoring other tests. In conclusion, this review of 115 patients who underwent needle aspiration biopsy for cytologic study of palpable breast masses reaffirms the usefulness of the technique. Because of a small but definite incidence of false-positive results, total mastectomy cannot be recommended based on cytologic findings alone. The sensitivity and overall accuracy rate was 92 percent, the specificity rate was 97 percent, and the predictive value was 92 percent, demonstrating that the setting of a residency training program does not adversely affect the reliability of the technique. REFERENCES 1. Halvey A, Reif R, Bogokovsky H, Orda R. Diagnosis of carcinoma of the breast by fine needle aspiration. Surg Gynecol Obstet 1987; 164: 506-8. 2. Watson D, McGuire M, Nicholson F, Given H. Aspiration cytology and its relevance to the diagnosis of solid tumors of the breast. Surg Gynecol Obstet 1987; 165: 435-41. 3. Somers RG, Young GP, Kaplan M J, Bernhard VM, Rosenberg M, Somers D. Fine needle aspiration biopsy in the management of solid breast tumors. Arch Surg 1985; t20: 673-7. 4. Barrows G, Anderson M, Lamb M, Dixon J. Fine needle aspiration of breast cancer. Cancer 1986; 58: 1493-8. 5. Griffith C, Kern W, Mikkelsen W. Needle aspiration cytologic examination in the management of suspicious lesions of the breast. Surg Gynecol Obstet 1986; 162: 142-4. 6. Wanebo H, Feldman P, Wilhelm M, Covell J, Binns R. Fine needle aspiration cytology in lieu of open biopsy in management of primary breast cancer. Ann Surg 1984; 199: 569-79. 7. Ellis M, Ellis E. Biopsy by needle puncture and aspiration. Ann Surg 1930; 92: 169-81. 8. Goodson W, Mailman R, Miller T. Three year follow-up of benign fine-needle aspiration biopsies of the breast. Am J Surg 1987; 154: 58-61.
DISCUSSION Robert B. Sawyer (Denver, CO): In this series, every patient was biopsied. This is important because this technique will be attractive to the nonsurgeon. We must stress the need for tissue confirmation. Also, needle aspiration biopsy was performed at the time of initial contact with the patient. This is the time to begin discussing various options for handling breast malignancy and to give the patient a chance to make some decisions. Finally, the
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cytopathologist was present and the pathologist was dedicated to this technique. Dr. Kahky, my question is, how do you have the cytopathologist adjacent to your clinic? Is he around all the time with you? Is the clinical setting a breast tumor clinic, which really isn't the initial patient contact? Another question I have is, what about the patient who decides to have a modified radical mastectomy with a suspicious needle bioPsY? Do you perform this under local anesthesia and then ask her if she really wants to go through with the mastectomy? This is a very sensitive time, and faced with the reality of cancer, the patient may favor lumpectomy. Kent C. Westbrook (Little Rock, AR): If needle . aspiration biopsy is really going to be of value, we are going to have to get good enough to operate if positive cytologic findings are combined with typical clinical and mammographic findings. Dr. Kahky, when, if ever, would you be willing to do a mastectomy under these circumstances? John Ferrara (Mobile, AL): The main advantage of fine-needle aspiration is that positive cytologic findings allow you to talk with the patient about surgical options before proceeding with any definitive care, including biopsy. We think this is particularly important since many patients will select partial mastectomy. Nonetheless, I am still not willing to accept positive cytologic findings as the final word. I believe that biopsy with frozen section analysis is indicated for all patients prior to carrying out definitive surgery. Even one false-positive finding of fine-needle aspiration biopsy that leads to a more radical operation than is necessary is too much for meto accept. Dr. Kahky, I think the false-negative rate you reported is a little low and the false-positive rate is too high. Michael P. Kahky (closing): Dr. Sawyer, we have a cytotechnologist who regularly attends the breast clinic and is in charge of preparing the slides. We do not perform biopsy followed by mastectomy at the same time because we believe that it is important for the pathologist to have time to review the entire slide and to make additional sections, if necessary. Drs. Westbrook and Ferrara, we think that needle aspiration biopsy is helpful because it allows us the opportunity to discuss therapeutic alternatives early in our encounter with patients, w e are not willing to go ahead with mastectomy based on positive cytologic findings; however, we do use this information to guide placement of the incision for open biopsy. If the cells are benign, we perform open biopsy through a circumareolar incision. In patients with suspicious cells who choose partial mastectomy, we place the incision away from the nipple-areolar complex.
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