Surgical specimens of either lumpectomy (40 specimens) or mastectomy or (quadrentectomy) (78 specimens) were cut into serial 5-mm slices that were considered as a reference standard according to the method of Egan. Grading of invasive ductal carcinoma was carried out according to the Nottingham system and that of duct carcinoma in situ (DCIS) was carried out according to the cytonuclear grade with specification of different variants of benign and malignant breast lesions.
One hundred and ten female patients were enrolled in this study; 78 of these patients older than 45 years of age, 26 patients were between 35 and 45 years of age, and only six patients were younger than 35 years of age. The possible risk factors, sides, size of lesions, and the results of clinical breast examination (CBE) are shown in Table 2.
On applying digital mammography, four other clinically missed contralateral lesions were discovered in four patients in addition to six small masses in patients with nipple retraction. Thus, a total of 118 masses were found in 110 patients; of the clinically 84 malignant masses, 74 were positive for malignancy and 10 were negative, whereas of the 34 clinically diagnosed benign masses, 26 masses, in addition to the four masses discovered radiologically, were true benign and four were malignant and proved to be false negative.
FNAC was performed in 74 cases; 52 were radiologically suspected as malignant and with FNAC, 50 were malignant and two cases were benign. Twenty-two cases were radiologically suspected as benign but with FNAC, 20 were benign and two cases were malignant, which was confirmed by an open biopsy.
CNB was performed in 44 cases; 30 were radiologically suspected as malignant and with CNB, 28 were malignant and two cases were benign. Fourteen cases were radiologically suspected as benign but with CNB, 12 were benign and two cases were malignant, which was confirmed by an open biopsy.
On additionally using the mini-invasive techniques, from the 86 cases radiologically diagnosed as malignant, 78 were positive and four lesions were negative and from the 28 cases that were radiologically negative, four were diagnosed as positive and 32 were negative. Therefore, there were 82 malignant cases and 36 negative cases.
By excision biopsy or radical mastectomy, four of the 36 negative lesions by the mini-invasive diagnosis were found to be positive and four of the 82 positive were found to be negative.
Therefore, 32 (27.12%) breasts were diagnosed histologically as negative and 86 specimens (72.88%) were proved to be malignant (78 from the malignant and four out of these benign by mini-invasive techniques). The end result of each procedure is shown in Table 3.
Malignant lesions were as follows: DCIS in two, invasive ductal carcinoma in 52, invasive lobular carcinoma in 14, medullary carcinoma in six, tubular carcinoma in two, papillary carcinoma in two, mucinous carcinoma in two, and malignant phylloides in two cases (Fig. 2).
Benign lesions were fibroadenoma in 16, benign phylloides in two, adenosis in 14, mastitis in two, and fat necrosis in two.
Accurate preoperative diagnosis of breast carcinoma is necessary in screen-detected lesions so that patients may be counseled appropriately, and a majority may require a single therapeutic operation (Lieske et al., 2006).
To compare tests fairly, both FNAC and CNB should be taken from the same lesion that is later surgically excised for definitive histology. Both tests should be performed in the same sitting, ideally under the same guidance (clinical or US), and the operator should be skilled in both techniques. FNAC, especially, is more operator dependent than CNB. It is more difficult and painful for patients when both FNAC and CB are taken from the same lesion in the same sitting; the aim of our study was to evaluate the accuracy of FNAC and CNB separately or in combination with clinical and radiological assessment in the diagnosis of breast masses.
The cost of core biopsy is higher than that of FNAC, but the former provides adequately sized samples, enabling a histological diagnosis, allowing, for example, the differentiation between in-situ and invasive carcinoma. CNB samples can also be used in immunohistochemical assays of hormone receptor and other prognostic tumor markers (Ricci et al., 2012). In our study, the cell blocks obtained by FNAC could also be utilized for hormonal assays; moreover, Pegolo et al. (2012) found a high level of agreement between thin preparation cytology and tissue samples in terms of the evaluation of estrogen and progesterone receptors as HER2. However, FNAC is one of the most common methods for the diagnosis of small solid breast lesions because it is simple, quick, low cost, and safe. Moreover, patients usually tolerate FNAC well as it causes minimal pain and bleeding (Sauer et al., 2005).
There was no reported complication in all 110 cases described in our series. The age range (29–63 years) of the patients was comparable with that in the studies of Lee et al. (2003), Berg et al. (2004), and Chagpar et al. (2006), in which age ranges of the patients were 28–75, 26–81, and 27–74 years, respectively.
CBE is the best noninvasive predictor of the actual size of palpable breast cancer (Lee et al., 2003) and is relatively simple and inexpensive, but with high false-positive results (Anna et al., 2009). Mammography is complex, expensive, and only partially effective. There is sufficient circumstantial evidence to suggest that CBE is as effective as mammography in reducing mortality from breast cancer (Mittra et al., 2000). In our study, mammography was more reproducible than CBE, where the former had 90.7% sensitivity, 87.5% specificity, 90.7% positive predictive value (PPV), 87.5% negative predictive value (NPV), and 89.5% accuracy, whereas the latter (CBE) had 88.1% sensitivity, 76.5% specificity, 88.1% PPV, 76.5% NPV, and 84.7% accuracy.
In our study, the size of palpable lesions ranged from 0.8 to 3.5 cm; in 80 cases, the tumor sizes were clinically more than 2 cm and in 38 cases the sizes were less than 2 cm, with an accuracy of 84.7%. After imaging procedures, the accuracy increased to 89.8%. The difference was not essentially significant. In the study of Chagpar et al. (2006), the accuracy was moderately correlated with pathologic tumor size, where an accuracy of 66% was obtained by physical examination, 75% by US, and 70% by mammography.
The sensitivity of digital mammography for breast tumors was 90.7%, which is comparable with the 96.7% reported in the Cockcroft’s (2005) study in contrast to the Berg et al.’s (2004) study, in which mammography was relatively insensitive to all cancers in dense breasts (32%).
It was also noted that sensitivity was affected by breast density. In our study, of the 38 fatty breasts, there were 26 cancers (68.42%) and out of the 80 dense breasts, there were 58 cancers (72.5%), with a total sensitivity of 90.7%. Digital mammography detected 24 cancers in fatty breasts, representing 63% accuracy, and 62 cancers in dense breasts, representing 77.5% accuracy, with a total sensitivity of 95%. In Oestreicher et al.’s (2005) study, the sensitivity of mammography was 78%.
When comparing the sensitivity, specificity, PPV, NPV, and accuracy of CBE, radiological diagnosis, and mini-invasive diagnosis, our results showed that sensitivity was 88.1, 90.7, and 95.1%; specificity was 76.5, 87.5, and 88.9%; PPV was 88.1, 90.7, and 95.1%; NPV was 76.5, 87.5, and 88.9%; and accuracy was 84.7, 89.8, and 93.2%, respectively.
In our study, the false-positive rate of FNAC was 3.84%, whereas the false-negative rate of FNAC was 9.09%. The false-negative rate of FNAC has been reported to range from 2 to 18% by Domínguez et al. (1997), and the false-positive rate was 0.3–1.6% as reported by Bell et al. (1983), Silverman et al. (1987), and Domínguez et al. (1997). In the study of Pinto and Singh (1992), the false-negative rate was 1.3%. Singh et al. (2003), over a 4-year period, on correlating 67 of their FNAC cases with their subsequent histopathology, 6.1% of them were false negative.
The sensitivity, specificity, and accuracy of FNAC for breast tumors ranged from 82 to 98%, from 77 to 100%, and from 79 to 97%, respectively, in several studies (Arisio et al., 1998; Ishikawa et al., 2007; Nguansangiam et al., 2009). In our study, FNAC of palpable breast lesions showed a sensitivity of 96.2%, a specificity of 90.9%, and an accuracy of 94.6%. The PPV was 96.2% and the NPV was 90.9%. These results are in agreement with many other reports that have shown the high diagnostic value of this technique (Ariga et al., 2002; Medina Franco et al., 2005; Ishikawa et al., 2007; Nguansangiam et al., 2009). However, in the Rosa et al.’s (2012) study, FNAC showed a sensitivity of 92%, a specificity of 100%, and an accuracy of 94%. The PPV was 100% and the NPV was 79%, and in the Bukhari and Akhtar’s (2009) study, the sensitivity, specificity, accuracy, PPV, and NPV of FNAC were 97, 100, 97, 100, and 87%, respectively.
Although CNB has high quality, factors such as degree of nodularity; thickening versus a mass; dimpling of skin; or the size, mobility, shape, or consistency of an abnormality have to be considered. In our study, the false-positive rate in CNB was higher than FNAC: 6.66 and 3.84%, respectively; this was not in agreement with the study of Fenton et al. (2005), who reported that CNB was better than FNAC and physicians might require training in performing high-quality CNB.
In agreement with our results, Oestreicher et al. (2005) and Anna et al. (2009) reported that CNB led to a higher risk of false-positive results and they recommended standardization of interpretation and reporting. The balance of risks and benefits, which were greater in dense breasts, must be weighed carefully when evaluating the inclusion of either FNAC or CNB in a screening examination (Saslow et al., 2004).
In our study, statistical results of the pathologic examination of FNAC and CNB showed 96.2 and 93.3% sensitivity, 90.9 and 85.7% specificity, 96.2 and 93.3% PPV, 90.9 and 85.7% NPV, and 94.6 and 91.0% accuracy, respectively. Even if CNB showed adequate tissue sampling, its intrinsic disadvantage in terms of limited pathological sensitivity, specificity, PPV, NPV, and accuracy renders it inferior to FNAC. Experience from all over the world has shown that the additional costs to prove an FNAC over-call lesion to be benign is unavoidable in patients who could have undergone core biopsy (Mak et al., 2012).
In contrast to our study, some studies in palpable lesions have generally used automated CNB devices with relatively larger needle sizes and found CNB to be more sensitive. When both tests were performed clinically in palpable lesions, the sensitivity of FNAC varied from 90 to 98% and that of CNB varied from 90 to 100% (Ballo and Sneige, 1996; Agarwal et al., 2003; Dennison et al., 2003).
When both tests were performed under ultrasound guidance, some found the sensitivity of the FNAC to be equal to that of CNB (Hatada et al., 2000; Westenend et al., 2001), whereas others found CNB to be better (Chuo and Corder, 2003).
In the studies of Pilgrim and Ravichandran (2005) and Lieske et al. (2006), FNAC did not provide useful additional information owing to the correct diagnosis of almost all cancers by CNB, leaving little room for FNAC to improve upon the preoperative diagnosis rate.
Fewer comparison studies of a similar nature have been reported with screen-detected breast cancers. In an early study of 76 cancers, FNAC showed better complete sensitivity and less absolute sensitivity than CNB, but all sensitivities were generally low (32–72%) (Dowlatshahi et al., 1991). In another study of single-pass FNAC and CNB in 65 nonpalpable breast cancers (Lifrange et al., 1997), FNAC was inadequate in 22% and benign in 34%. The corresponding figures for CNB were 3 and 38%. It is now known that a minimum of five, often more, cores are necessary, especially with microcalcification, to reduce the number of inadequate specimens and false-negatives (Liberman et al., 1994; Romanelli and Smith, 1999; Michell, 2000). In a study of 81 carcinomas presenting as microcalcification, complete sensitivity of stereotactic FNAC (≤3 passes) was 65% compared with 97.5% for CNB (Newman et al., 2001).
In our locality, in particular, because of the increasing incidence of breast cancer, and generally, in the developing countries, because of shortage of the economic resources and to optimize cost effectiveness, FNAC is a very useful test, relatively rapid and inexpensive, less invasive owing to a finer needle size, and is easier/safer in certain lesions, such as very small lesions, lesions just under the skin, or those very close to the chest wall compared with CNB. FNAC maintains tactile sensitivity and allows multidirectional passes, enabling a broader sampling of the lesion and immediate reporting where necessary as well as hormone receptors assays. In addition, CNB is not used widely because of its complications, interpretation, and time-consuming results; therefore, palpable breast lesions can be diagnosed accurately only by a triple test (FNAC, physical examination, and mammography).
Conflicts of interest
There are no conflicts of interest.
Agarwal T, Patel B, Rajan P, Cunningham DA, Darzi A, Hadjiminas DJ.Core biopsy versus FNAC for palpable breast cancers. Is image guidance necessary?Eur J Cancer2003;39:52–56.
Anna MC, Fornage BD, Singletary E.Contribution of clinical breast examination to breast cancer screening.J Natl Cancer Inst2009;101:1221–1226.
Ariga R, Bloom K, Reddy VB, Kluskens L, Francescatti D, Dowlat K, et al..Fine-needle aspiration of clinically suspicious palpable breast masses with histopathologic correlation.Am J Surg2002;184:410–413.
Arisio R, Cuccorese C, Accinelli G, Mano MP, Bordon R, Fessia L.Role of fine-needle aspiration biopsy in breast lesions: analysis of a series of 4,110 cases.Diagn Cytopathol1998;18:462–467.
Ballo MS, Sneige N.Can core needle biopsy replace fine-needle aspiration cytology in the diagnosis of palpable breast carcinoma: a comparative study of 124 women.Cancer1996;78:773–777.
Bell DA, Hajdu SI, Urban JA, Gaston JP.Role of aspiration cytology in the diagnosis and management of mammary lesions in office practice.Cancer1983;51:1182–1189.
Berg WA, Gutierrez L, NessAiver MS, Carter WB, Bhargavan M, Lewis RS, Ioffe OB.Diagnostic accuracy of mammography, clinical examination, US, and MR imaging in preoperative assessment of breast cancer.Radiology2004;233:830–849.
Bukhari MH, Akhtar ZM.Comparison of accuracy of diagnostic modalities for evaluation of breast cancer with review of literature.Diagn Cytopathol2009;37:416–424.
Chagpar AB, Middleton LP, Sahin AA, Dempsey P, Buzdar AU, Mirza AN, et al..Accuracy of physical examination, ultrasonography, and mammography in predicting residual pathologic tumor size in patients treated with neoadjuvant chemotherapy.Ann Surg2006;243:257–264.
Chuo CD, Corder AP.Core biopsy versus fine needle aspiration cytology in a symptomatic breast clinic.Eur J Surg Oncol2003;29:374–378.
Coburn NG, Chung MA, Fulton J, Cady B.Decreased breast cancer tumor size, stage, and mortality in Rhode Island: an example of a well-screened population.Cancer Control2004;11:222–230.
Cockcroft J2005How important is clinical examination in the diagnosis of breast cancer? Breast Cancer Audit Project 1–9..
Dennison G, Anand R, Makar SH, Pain JA.A prospective study of the use of fine-needle aspiration cytology and core biopsy in the diagnosis of breast cancer.Breast J2003;9:491–493.
Domínguez F, Riera JR, Tojo S, Junco P.Fine needle aspiration of breast masses: an analysis of 1,398 patients in a community hospital.Acta Cytol1997;41:341–347.
Dowlatshahi K, Yaremko ML, Kluskens LF, Jokich PM.Nonpalpable breast lesions: findings of stereotaxic needle-core biopsy and fine-needle aspiration cytology.Radiology1991;181:745–750.
Fenton JJ, Barton MB, Geiger AM, Herrinton LJ, Rolnick SJ, Harris EL, et al..Screening clinical breast examination: how often does it miss lethal breast cancer?J Natl Cancer Inst Monogr2005;35:67–71.
Fishman JE, Milikowski C, Ramsinghani R, Velasquez MV, Aviram G.US-guided core-needle biopsy of the breast: how many specimens are necessary?Radiology2003;226:779–782.
Fracheboud J, Otto SJ, Van Dijck JAMM, Broeders MJM, Verbeek ALM, De Koning HJ.Decreased rates of advanced breast cancer due to mammography screening in the Netherlands.Br J Cancer2004;91:861–867.
Hansen NM, Growney A.Breast cancer: pre- and postoperative imaging for staging.Surg Oncol Clin N Am2007;16:447–463.
Hatada T, Ishii H, Ichii S, Okada K, Fujiwara Y, Yamamura T.Diagnostic value of ultrasound-guided fine-needle aspiration biopsy; core-needle biopsy; and evaluation of combined use in the diagnosis of breast lesions.J Am Coll Surg2000;190:299–303.
Ishikawa T, Hamaguchi Y, Tanabe M, Momiyama N, Chishima T, Nakatani Y, et al..False-positive and false-negative cases of fine-needle aspiration cytology for palpable breast lesions.Breast Cancer2007;14:388–392.
Jay H, Monica M, Marce L, Samuel H.Disease of the breast1996.Philadelphia:Lippincott Williams & Wilkins.
Lee SG, Orel SG, Woo IJ, Cruz Jove E, Putt ME, Solin LJ, et al..MR imaging screening of the contralateral breast in patients with newly diagnosed breast cancer: preliminary results.Radiology2003;226:773–778.
Liberman L, Dershaw DD, Rosen PP, Abramson AF, Deutch BM, Hann LE.Stereotaxic 14-gauge breast biopsy: how many core biopsy specimens are needed?Radiology1994;192:793–795.
Lieske B, Ravichandran D, Wright D.Role of fine-needle aspiration cytology and core biopsy in the preoperative diagnosis of screen-detected breast carcinoma.Br J Cancer2006;95:62–66.
Lifrange E, Kridelka F, Colin C.Stereotaxic needle-core biopsy and fine-needle aspiration biopsy in the diagnosis of nonpalpable breast lesions: controversies and future prospects.Eur J Radiol1997;24:39–47.
Mak WS, Fong CY, Lui CY.Ultrasound-guided biopsy of solid breast lesions: Should fine-needle aspiration be replaced by core biopsy?Hong Kong J Radiol2012;15:10–14.
Medina Franco H, Abarca Pérez L, Cortés-González R, Soto-Germes S, Ulloa JA, Uribe N.Fine needle aspiration biopsy of breast lesions: institutional experience.Rev Invest Clin2005;57:394–398.
Michell MDixon JM.FNAC and core biopsy of impalpable lesions.In breast cancer: diagnosis and management2000:1st ed.Elsevier;31–41.
Mittra I, Baum M, Thornton H, Houghton J.Is clinical breast examination an acceptable alternative to mammographic screening?Br Med J2000;321:1071–1073.
Newman MR, Frost FA, Sterrett GF, Bourke AG, Thompson RI, Hastrich DJ, Ingram DM.Diagnosis of breast microcalcifications: a comparison of stereotactic FNA and core imprint cytology as adjuncts to core biopsy.Pathology2001;33:449–453.
Nguansangiam S, Jesdapatarakul S, Tangjitgamol S.Accuracy of fine needle aspiration cytology from breast masses in Thailand.Asian Pac J Cancer Prev2009;10:623–626.
Oestreicher N, Lehman CD, Seger DJ, Buist DSM, White E.The incremental contribution of clinical breast examination to invasive cancer detection in a mammography screening program.Am J Roentgenol2005;184:428–432.
Oz A, Demirkazik FB, Akpinar MG, Soygur I, Baykal A, Onder SC, Uner A.Efficiency of ultrasound and ultrasound-guided fine needle aspiration cytology in preoperative assessment of axillary lymph node metastases in breast cancer.J Breast Cancer2012;15:211–217.
Pegolo E, Machin P, Riosa F, Bassini A, Deroma L, Di Loreto C.Hormone receptor and human epidermal growth factor receptor 2 status evaluation on ThinPrep specimens from breast Carcinoma: correlation with histologic sections determination.Cancer Cytopathol2012;120:196–205.
Pilgrim S, Ravichandran D.Fine needle aspiration cytology as an adjunct to core biopsy in the assessment of symptomatic breast carcinoma.Breast2005;14:411–414.
Pinto RG, Singh K.A statistical analysis of fine needle aspiration biopsies done in palpable breast lesions.J Cytology1992;20:189–192.
Ricci MD, Filho CMCC, Filho HRO, Filassi JR, Pinotti JA, Baracat EC.Analysis of the concordance rates between core needle biopsy and surgical excision in patients with breast cancer.Rev Assoc Med Bras2012;58:532–535.
Romanelli JR, Smith TJ.Management of nonpalpable breast lesions: techniques in breast biopsy.Cancer Invest1999;17:624–630.
Rosa M, Mohammadi A, Masood S.The value of fine needle aspiration biopsy in the diagnosis and prognostic assessment of palpable breast lesions.Diagn Cytopathol2012;40:26–34.
Salhia B, Tapia C, Ishak EA, Gaber S, Berghuis B, Hussain KH, et al..Molecular subtype analysis determines the association of advanced breast cancer in Egypt with favorable biology.BMC Women’s Health2011;11:44.
Saslow D, Hannan J, Osuch J, Alciati MH, Baines C, Barton M, et al..Clinical breast examination: practical recommendations for optimizing performance and reporting.CA Cancer J Clin2004;54:327–344.
Satchithananda K, Fernando RA-M, Ralleigh G, Evans DR, Wasan RK, Bose S, et al..An audit of pain/discomfort experienced during image-guided breast biopsy procedures.Breast J2005;11:398–402.
Sauer T, Løma J, Garred Ø, Næss O.Cytologic features of ductal carcinoma in situ in fine-needle aspiration of the breast mirror the histopathologic growth pattern heterogeneity and grading.Cancer2005;105:21–27.
Silverman JF, Lannin DR, O’Brien K, Norris HT.The triage role of fine needle aspiration biopsy of palpable breast masses: diagnostic accuracy and cost-effectiveness.Acta Cytol1987;31:731–736.
Singh K, Dubey VK, Khajuria R.Diagnostic accuracy of fine needle aspiration cytology when compared with histopathology.J Cytol2003;20:22–27.
Verkooijen HM.Diagnostic accuracy of stereotactic large-core needle biopsy for nonpalpable breast disease: results of a multicenter prospective study with 95% surgical confirmation.Int J Cancer2002;99:853–859.
Vlastos G, Verkooijen HM.Minimally invasive approaches for diagnosis and treatment of early-stage breast cancer.Oncologist2007;12:1–10.
Westenend PJ, Sever AR, Beekman-de Volder HJC, Liem SJ.A comparison of aspiration cytology and core needle biopsy in the evaluation of breast lesions.Cancer2001;93:146–150.
.World Health Organization Cancer Control Programme Department of Chronic Diseases and Health Promotion (CHP)2012.Geneva, Switzerland:World Health Organization.
©2013Egyptian Journal of Pathology
Yu Y-H, Wei W, Liu J-L.Diagnostic value of fine-needle aspiration biopsy for breast mass: a systematic review and meta-analysis.BMC Cancer2012;12:41.