The World Health Organization (2012) has ranked breast cancer as the most common type of cancer among women worldwide. The incidence rates of breast cancer vary worldwide; according to GLOBOCAN 2008, breast cancer accounts for 38% of all new cancer cases among women living in Egypt. Mortality rates in Egypt are worse (20.1/100 000) than they are in the USA (14.7/100 000), and breast cancer is the leading cause of cancer-related deaths (Salhia et al., 2011).
Palpable breast mass is a common problem in female patients. The diagnostic delays of breast cancer occur because of the generally low index of suspicion. The traditional diagnosis mode of breast mass is excision biopsy, which provides a precise diagnosis, but may yield a benign pathological result in most cases (Yu et al., 2012).
Fine-needle aspiration cytology (FNAC) is a well-established tool for the evaluation of palpable breast lumps, but is less suitable for the diagnosis of nonpalpable breast disease. FNAC allows the pathologist to identify the presence of malignant cells but not to distinguish between invasive and in-situ cancer (Vlastos and Verkooijen, 2007).
The limitations of FNAC have led to the introduction of large-core needle biopsy (CNB) for the diagnostic workup of nonpalpable breast lesions. With CNB, actual tissue samples are obtained using a large-core needle (generally 14 G) and an automated biopsy gun (Fishman et al., 2003).
The diagnostic accuracy of CNB is high: miss rates of cancer vary from 1 to 7%, whereas false-positive findings are very rare (Verkooijen, 2002). Core biopsy is generally considered as a better alternative to FNAC in terms of lower rates of inadequate sampling and having an accuracy comparable to that of excision biopsy (Satchithananda et al., 2005).
With the introduction of ultrasonographically (US)-guided methods for nonpalpable lesions, FNAC and CNB have been used more widely in the evaluation of nonpalpable breast lesions (Oz et al., 2012).
Mammography is still considered the ‘gold standard’ in the evaluation of the breast from an imaging perspective. Multiple studies have shown the benefit of mammography in the detection of smaller cancers, leading to identification of early-stage breast cancers, which largely accounts for decreased mortality rates from breast cancer (Coburn et al., 2004; Fracheboud et al., 2004; Hansen and Growney, 2007).
Furthermore, the triple-diagnostic method [consisting of clinical evaluation, mammography, and minimally invasive histopathological techniques (FNAC and CNB)] provides a precise diagnosis and reduces the risk of missed diagnosis of breast cancer to less than 1% (Jay et al., 1996).
Therefore, the aim of our study is to evaluate the accuracy of minimal invasive techniques separately or in combination with clinical and radiological assessment in the diagnosis of breast masses.
Patients and methods
This prospective study was carried out in collaboration between the Department of Pathology, Mansoura Faculty of Medicine, and the Departments of Surgery and Radiology, Al-Azhar Faculty of Medicine (Damietta Hospital). A total of 110 female patients were enrolled; 104 presented with hard breast lumps (62 in the left side, 42 in the right side) and six patients presented with nipple retractions (four left and two right) during the period from October 2007 to December 2010. The ages of patients ranged between 29 and 63 years.
Clinical breast examination
All patients were subjected to assessment of clinical history with a focus on the risk factors and general and local examinations. Local examination including visual inspection and palpation of every area of the breast and surrounding tissue indicated bilateral lesions in four patients. The step of the clinical examination duration ranged between 8 and 15 min. The lymph nodes in the axillae and clavicular areas were examined.
On the basis of clinical findings, digital mammography of bilateral whole breast was performed using a linear-array broadband transducer with a center frequency of 10 MHz and a linear-array transducer with a center frequency of 7.5 MHz as needed to penetrate larger breasts. The inner breast was scanned with the patient in the supine position and the outer breast was scanned by placing the patient in the contralateral posterior oblique position with a raised ipsilateral arm (both in transverse and sagittal planes). Lesions were measured in both radial and antiradial scanning planes.
Before the FNAC and core biopsy, previous ultrasound images available for all the women were reviewed to localize the target lesion. A written consent was obtained from all patients before the biopsy was performed for all palpable solid masses and for the 10 incidental solid masses discovered by digital mammography (six patients with nipple retraction and four contralateral sides) guided by the US.
FNAC was performed in 74 cases, and six of these were performed under US guidance using a 21 G needle attached to a 10 ml disposable syringe. When FNAC was performed, one to two passes were routinely performed. A local anesthetic was not used. The aspirated material sufficiency was tested by quick staining (within 1 min) with methylene blue stain to minimize the false-negative results and repetition of the process. Four to six slides were prepared and fixed in 90% ethyl alcohol and the other two were dried. The smears were stained with hematoxylin and eosin and Papanicolaou stains. The remaining aspirates were fixed in 10% neutral-buffered formalin for cell block preparation to be used for hormone receptors assays later. The entire procedure until final reporting was performed within 2–3 h.
CNBs were performed in 44 cases; four of these were performed under US guidance in the contralateral breast lesions. CNB was performed using an automated device (14 G, 14 mm stroke margin, Pro-Mag 1.4; MDTech Inc., Gainesville, USA), fixed in 10% neutral-buffered formalin, processed and paraffin-embedded, cut at 4–5 μm, and stained with hematoxylin and eosin. The outcomes of FNAC and CNB were reported using the standard National Health Service Breast Screening Program (HSBSP) criteria (Table 1); the standard cytological and histological criteria of benign and malignant lesions and their special variants were also reported (Fig. 1).
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.
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