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Year : 2014  |  Volume : 11  |  Issue : 1  |  Page : 36-40

Validity of fine needle aspiration cytology of the palpable breast lesions: A teaching hospital experience

Department of Pathology, Aminu Kano Teaching Hospital/Faculty of Medicine, Bayero University, Kano, Nigeria

Date of Web Publication7-Apr-2014

Correspondence Address:
Ibrahim Yusuf
Department of Pathology, Aminu Kano Teaching Hospital, 3452, Kano - 700001
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0331-8540.130170

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Background and Objective: Fine needle aspiration cytology has assumed a great importance in the pre-operative diagnosis of palpable breast lesions in several hospital and clinical settings worldwide. This study aims to audit its diagnostic utility and validity in a tertiary hospital, and to review some of the diagnostic pitfalls in interpretation of breast cytology. Materials and Methods: The study comprised of breast cytology reports and their subsequent tissue biopsy diagnoses recorded over a 5-year period from January 2008 to December 2012. Results: A total of 1162 breast cytology reports were made over the review period out of which 200 had histological confirmation. Out of the 200 cases, 109 (54.5%) were benign (C2), 20 (10.0%) cases were suspicious probably benign (C3), 27 (13.5%) cases were suspicious probably malignant (C4) and 44 (22.0%) were malignant (C5). The cytology reports were correlated with subsequent histological diagnoses. Of the 109 benign C2 reports, 99 were confirmed on tissue histology as truly benign (true negatives) and the remaining 10 cases were malignant (false negatives). Forty-three of the 44 malignant (C5) cytology reports initially made were confirmed as malignant on tissue histology (true positives). The remaining malignant (C5) cytology case was, however, revealed to be benign (false positive). The overall suspicious rate (C3 and C4) was 23.5%. The absolute sensitivity was 81.0%, specificity was 99.0%, positive predictive value (PPV) (C5) of 97.7%, negative predictive value (NPV) (C2) of 90.8%. The false positive rate (FPR), false negative rate (FNR) and suspicious rates (SR) were 1.2%, 12.0% and 23.5%, respectively. Conclusion: Fine needle aspiration cytology of the breast has recorded high absolute sensitivity and specificity in our centre with a marginally high false positive rate. It has thus continued to have relevance as an important pre-operative diagnostic tool in the management of palpable breast lesions in our hospital.

Keywords: Breast, cytology, predictive value, sensitivity, specificity, suspicious

How to cite this article:
Yusuf I, Atanda A T. Validity of fine needle aspiration cytology of the palpable breast lesions: A teaching hospital experience. Niger J Basic Clin Sci 2014;11:36-40

How to cite this URL:
Yusuf I, Atanda A T. Validity of fine needle aspiration cytology of the palpable breast lesions: A teaching hospital experience. Niger J Basic Clin Sci [serial online] 2014 [cited 2023 Feb 5];11:36-40. Available from: https://www.njbcs.net/text.asp?2014/11/1/36/130170

  Introduction Top

The role of non-operative techniques in definitive diagnosis of malignancy is to enable rapid referral for treatment, ideally in one operative procedure. [1] Fine needle aspiration cytology (FNAC) of the breast, as part of the triple approach to the diagnoses of palpable breast lesions, has become a valuable pre-operative tool. It is fast, inexpensive and minimally invasive and thus has gained wide acceptance in the pre-operative assessment of breast lesions. FNAC of the breast has two main goals; to confirm radiological and clinically benign lesions thus avoiding unnecessary surgery, and to confirm radiological and clinically malignant diagnoses thus enabling definitive treatment planning. [2] In this regard, breast cytology has been shown to be highly sensitive and specific. [3]

The evaluation of cytological criteria used to differentiate benign from malignant lesions has revealed a significant overlap, particularly in cases of fibroadenoma and proliferative breast diseases. [4] In order to address these areas of cyto-morphologic uncertainties, and to ensure uniformity in the diagnostic reporting, the National Cancer Institute (NCI) [5] has developed and recommended five categories for assessing and reporting palpable breast lesions. The five categories for reporting of these lesions include: Inadequate smear (C1), benign (C2), suspicious probably benign (C3), suspicious probably malignant (C4) and malignant (C5).

The subcategories diagnosed as atypical (C3 and C4) have similar probabilities of malignancy. This justifies their being grouped as a single category where tissue biopsy is required to exclude carcinoma. Benign (C2) and inadequate (C1) cytology reports must be correlated with clinical and imaging findings. Where disparity exists, the patient should undergo tissue biopsy. [2],[6]

Smears are designated inadequate (C1) if they show marked hypocellularity, haemorrhage and artefacts to preclude microscopic diagnosis. When smears are adequate and representative, show no evidence of atypia or malignancy, demonstrates monolayer sheets of cells with benign cytological features and bare nuclei, they are categorised as benign (C2). Suspicious probably benign (C3) samples have all the features of benign aspirates in addition to features such as nuclear atypia, hypercellularity and discohesion not commonly seen in benign lesions. Smears with low cellularity and subtle cytological atypia are also grouped in this category. Cells with features suggestive of, but not diagnostic of malignancy and show degree of abnormality greater than the previous category (C3) are diagnosed as suspicious probably malignant (C4). In addition, this category also has an overall benign pattern. Malignant (C5) category show adequate samples that show unequivocal distinctly malignant features. [2]

We have been involved in the reporting of breast cytology aspirates using the NCI [2] guidelines for over a decade. There is need therefore to audit the performance of FNAC of the breast and assessing its degree of validity at detecting or excluding malignant breast lesions in our centre.

  Materials and Methods Top

The study was a retrospective review of cases of FNAC of palpable breast lesions performed over a 5-year period from 1 January 2008 to 31 December 2012. Aspirates were obtained using 23G needle using either free hand or attached to 20 ml syringe/syringe holder. Smears were fixed in 90% alcohol and/or air dried and stained with Papanicolaou and Diff Quik (giemsa) stains, respectively. Prepared slides were reviewed and reported according to NCI [5] guidelines. Only 200 cytology cases that had subsequent histological diagnoses were reviewed. The initial cytological reports were correlated with the final histological diagnoses. The validity of the results of the FNAC of the breast lesions in terms of sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) were calculated. The false positive rate (FPR), false negative rate (FNR) and the suspicious rate (SR) were also determined.

  Results Top

A total of 1162 cytology reports of palpable breast lesions were issued over the 5-year period of the study. Out of this number, 200 had subsequent tissue biopsies and histological diagnoses in the same hospital where the initial cytology reports were made. All inadequate (C1) smears were repeated by more experienced pathologist and reportable smears obtained and thus no C1 cases were documented.

A total of 200 cytology cases had histological confirmation. Of this, 109 (54.5%) were reported as benign (C2), 20 (10.0%) cases were suspicious probably benign (C3), 27 (13.5%) cases were suspicious probably malignant (C4) and 44 (22.0%) were malignant (C5).

The 200 cytology reports were correlated with their subsequent histological diagnoses. Of the benign C2 reports (109 cases), 99 were confirmed on tissue histology as truly benign (true negatives) and the remaining 10 were malignant (false negatives) [Table 1].
Table 1: Breast cytology results and corresponding histological outcomes

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Forty-three of the 44 malignant (C5) cytology reports initially made were confirmed by tissue histology to be actually malignant (true positives). The remaining malignant (C5) cytology case was, however, revealed to be benign (false positive) [Table 1].

Twenty (10.0%) cases of suspicious C3 and 27 (13.5%) cases of suspicious C4 cytology reports were made. Of the 20 cases of suspicious C3, 13 were benign and 7 were malignant on tissue histology. Twenty-seven suspicious (C4) cases were recorded and 23 of them turned out malignant. The overall suspicious rate (C3 and C4) was 23.5%.

The frequency distribution of the various benign and malignant histological subtypes and their initial cytological diagnoses are depicted in [Table 2] and [Table 3], respectively.
Table 2: Breast cytology results and corresponding subsequent benign histological diagnoses

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Table 3: Breast cytology results and corresponding subsequent malignant histological diagnoses

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Excluding the equivocal suspicious cytology reports (C3 and C4 cases) and correlating the definitive benign (C2) and malignant (C5) cytology reports (total of 153) with their confirmatory tissue diagnoses, the measure of accuracy of FNAC of the breast cytology were determined with absolute sensitivity of 81.0%, specificity of 99.0%, PPV (C5) of 97.7% and NPV (C2) of 90.8%. The FPR was 1.2% while the FNR was 12%.

The most common benign histological subtype was fibroadenoma (60.7%), followed by fibrocystic change (17.1%) and benign phyllodes (9.4%). The most frequent malignant histological subtype seen was invasive ductal carcinoma (69.9%) while the least common types included apocrine carcinoma, malignant phyllodes, tubular carcinoma and pleomorphic carcinoma [Table 2] and [Table 3].

  Discussion Top

FNAC of the palpable breast lesion has proven to be very useful in screening for breast pathology. [7] It has provided the surgeon with the enabling tool to decide on further mode of management of his patients. Records show that our centre has been involved in FNAC of the breast for over 14 years. This study reviewed cases seen over the past 5 years. The review recorded an absolute sensitivity of 81.0%, a specificity of 99.0%, a PPV (C5) of 97.7% and a NPV (C2) of 90.8%. These values satisfy the minimum requirement for breast cytology performance set by the UK National Health Service Breast Screening Pathology (NHSBSP). [8] The UK NHSBSP suggested a minimum threshold for breast cytology performance as thus: Absolute sensitivity >60%, complete sensitivity >80%, full specificity >55%, PPV >98%, FNR <6% and FPR <1%. However, the FPR and the FNR recorded by this study were relatively high at 1.2% and 12%, respectively.

The marginally high FPR might be attributable to cyto-morphological feature overlap of benign and malignant lesions and to errors of interpretation. [6],[8] The false positive case diagnosed on cytology was later reported as sclerosing adenosis and clear lactation changes were noted. Focal lactation changes in benign lesions can produce occasional discohesive cells, which may have larger nuclei and prominent nucleoli resulting in interpretation errors. [2],[8] In this case, history of lactation was neither volunteered by the referring physician nor elicited by the aspirator.

Fibroadenoma constituted the majority of benign tumours in the study. These tumours constitute the largest cause of false positive and false negative diagnoses. [2],[6],[8],[9] They may demonstrate cellular discohesion and marked pleomorphism, which can lead to falsely atypical or malignant diagnosis. [6],[8] This review recorded eight falsely atypical/suspicious cases. Despite the worrisome appearance fibroadenoma may exhibit, the clue to accurate diagnosis is the presence of stromal fragments (mucin) [2],[10] and stripped bipolar nuclei, which is a highly specific indicator of a benign process. [2],[6],[8],[9],[10]

Apocrine change in cytological smears may pose diagnostic difficulty and is seen in a wide variety of breast lesions including sclerosing adenosis, fibrocystic change and apocrine carcinoma. [6] Degenerate apocrine cells in cyst fluid may appear discohesive and pleomorphic thereby mimicking malignancy. [8] Differentiating fibrocystic change with atypical apocrine metaplasia or degenerate apocrine cells from low grade apocrine carcinoma can be difficult. [6] FNAC of apocrine carcinoma is highly cellular and shows marked nuclear atypia. Even though benign lesions may show degenerate apocrine cells or atypical apocrine metaplasia, they are usually less cellular. [6],[8],[9] If the fluid aspirate does not contain blood or debris and if there are no residual lump after evacuation of the fluid, there is practically no likelihood of malignancy. [10]

Distinguishing papilloma from intracystic papillary carcinoma is difficult [6],[8] and may not be possible on cytological grounds. [8] Infarcted papilloma may closely mimic intracystic papillary carcinoma and both lesions may show marked nuclear atypia, complex papillae and single cells, necrosis and inflammation. [6],[10] However, the findings of apocrine metaplasia and bipolar naked nuclei favour a benign diagnosis. [6] In general, a definitive cytological diagnosis of malignancy should not be made on papillary lesions. [2],[10]

Atypical ductal and lobular hyperplasia, lobular carcinoma in situ, lactation changes, blunt duct adenosis, fat necrosis, granulomatous mastitis and radiotherapy changes are other causes of false positive diagnoses. [6],[8],[10]

The most common cause of false negative is aspiration miss. [8] The high FNR recorded by this study may be predominantly due to sampling error and/or inadequate sampling. [7] In our centre, sampling of breast and other lesions are carried out routinely by trainee residents and this may contribute majorly to sampling errors. The success of FNAC is directly related to the skill and experience of the operators, hence trainees must be closely supervised. [8]

FNAC of invasive lobular carcinoma is associated with high FNRs and equivocal diagnosis. [6],[8],[10] This study documents two false negatives and three suspicious (equivocal) cases of invasive lobular carcinoma. Diagnostic dilemmas arise from hypocellularity of smears and benign looking appearance of the cells. However, large numbers of dispersed epithelial cells with intact cytoplasm exhibiting intracytoplasmic lumina, [6],[8],[10] nuclear irregularities, [6],[8] tendency to form single files and small clusters of cells with slightly enlarged nuclei are features aiding diagnosis. [6],[8] Other causes of false negative cytology include apocrine carcinoma, tubular carcinoma and ductal carcinoma in situ. [6],[8],[10]

An earlier study [11] in our centre recorded high complete sensitivity, specificity and FNR. The study also documents a high PPV (100%) as obtained by the index study justifying definitive surgery following malignant (C5) cytology. Boener et al.,[3] however, recorded lower rates of false positive and false negative diagnoses utilising ultrasound-guided FNAC of the palpable breast lesions perhaps highlighting their usefulness in decreasing sampling errors and inadequate smears and improving the validity of breast cytology.

Ngadda [12] et al., in Maiduguri, Nigeria, found a significantly higher sensitivity (97.7%) than obtained by this study and a comparable specificity of 98.8%. However, Alatise [13] et al., in Ibadan recorded lower sensitivity and specificity than those obtained in our centre. Both studies also had high FNR and FPRs. The suspicious (equivocal) rate determined by this study is 23.5%. Even though this relatively high suspicious rate limits the effectives of our FNAC of the breast, it is still within the range of 10-30% seen in most studies. [8]

All the international studies done [1],[14],[15] also obtained high sensitivity and specificity, thus highlighting the usefulness of FNAC as a pre-operative diagnostic tool in the management of palpable breast lesions. There is, however, decrease use of FNAC of the breast in the developed countries and in many institutions it has been replaced by core biopsies. [2],[6],[16],[17] However, most developing countries still utilise it either alone or as part of triple test approach to pre-operative diagnosis of palpable breast lesions.

In Nigeria, FNAC still remains the cheapest and fastest alternative for first line patient management. [13] This may be due to its relative cost effectiveness in relation to core needle and open biopsies. [2] Though some studies suggest core needle biopsy to be more accurate than FNAC, [16],[17] they are also more invasive, associated with greater potential for complications, consumes more time and are more expensive.

Multi-disciplinary triple step approach to pre-operative diagnosis is necessary to amplify the quality of FNAC of the breast and to decrease its diagnostic limitation. [18] A multi-disciplinary approach involving the pathologists, clinicians and radiologists ideally operating in a breast clinic will significantly improve the quality of pre-operative diagnoses of breast lesions in our institution.

  Conclusion Top

FNAC of palpable breast lesions in our centre records high sensitivity, specificity and predictive values. Particular attention to diagnostic pitfalls in interpretation of breast cytology will help in reducing the marginally high false rate recorded in our centre. We recommend its continued utilisation as a first line diagnostic modality in patients presenting with palpable breast lumps.

  References Top

1.Palombini L, Fulciniti F, Vetrani A, De Rossa G, Di Benedetto G, Zeppa P. Fine needle aspiration cytology of breast masses. A critical analysis of 1956 cases in 8 years (1976-84). Cancer 1988;6:2273-7.  Back to cited text no. 1
2.Berner A, Sauer T. Fine-needle aspiration of the breast. Ultrastruct Pathol 2011;35:162-7.  Back to cited text no. 2
3.Boerner S, Fornage BD, Singletary E, Sniege N. Ultrasound guided fine needle aspiration of non palpable breast lesion: Review of 1885 cases using the NCI-supported recommendation on the uniform approach to breast aspiration. Cancer 1999;87:19-24.  Back to cited text no. 3
4.Lim JC, Al-Masri H, Salhadar A, Xie HB, Gabram S, Wojcik EM. The significance of the diagnosis of atypia in breast fine needle aspiration. Diagn Cytopathol 2004;3:285-8.  Back to cited text no. 4
5.The uniform approach to breast fine-needle aspiration biopsy. National Cancer Institute Fine-Needle Aspiration of Breast Workshop Subcommittees. Diagn Pathol 1997;16:295-311.  Back to cited text no. 5
6.Kocjan G. Diagnostic dilemmas in FNAC cytology: Difficult breast lesions. In: Fine Needle Aspiration Cytology: Diagnostic Principles and Dilemmas. Ch. 9. Germany: Springer; p. 182-207.  Back to cited text no. 6
7.Mendoza P, Lacanbra M, Tan P, Tse GM. Fine needle cytology of the breast: The non malignant categories. Patholog Res Int 2011;2011:547580.  Back to cited text no. 7
8.Guidelines for non operative diagnostic procedures and reporting of breast cancer screening-Non-operative diagnosis subgroup of the national coordinating group for breast cancer screening pathology. NHSBSP Publication no 50; 2001.  Back to cited text no. 8
9.Lindholm K. Breast. In: Orell SR, Skerrette GF, Whitaker D. editors. Fine Needle Aspiration Cytology. 4 th ed. India: Elsevier; 2005. p. 215-7.  Back to cited text no. 9
10.Sturgis CD, Sethi S, Cajulis RS, Hidvegi DF, Yu GH. Diagnostic significance of 'benign pairs' and signet ring cells in fine needle aspirates (FNAs) of the breast. Cytopathology 1998;9:308-19.  Back to cited text no. 10
11.Mohammed AZ, Edino ST, Ochicha O, Alhassan SU. Value of fine needle aspiration in the preoperative diagnosis of palpable breast lumps in resource-poor countries: Nigerian experience. Ann Afr Med 2005;4:9-22.  Back to cited text no. 11
12.Ngadda HA, Tahir MB, Musa AB, Gali BM, Mavun AA, Pindiga UH, et al. Correlation between histopathologic and fine needle aspiration cytologic diagnosis of palpable breast: A 5 year review. Afr J Med Sci 2000;36:295-8.  Back to cited text no. 12
13.Alatise OI, Lawal OO, Olasode OO, Adesukanmi AR. Breast fine needle aspiration cytology in a Nigerian tertiary hospital. East Central Afr J 2006;12:126-32.  Back to cited text no. 13
14.Ariqa, R, Bloom K, Reddy BV, Klausken L, Francescatti D, Dowlat K, et al. Fine needle aspiration of clinically suspicious palpable breast masses with histopathological correlation. Am J Surg 2002;184:410-3.  Back to cited text no. 14
15.O'Neil S, Castelli M, Gattuso P, Klusken L, Madsen K, Aranha G. Fine-needle aspiration of 697 palpable breast lesions with histopathologic correlation. Surgery 1997;22:824-8.  Back to cited text no. 15
16.Lieske B, Ravichandran D, Wright D. Role of fine-needle aspiration and core biopsy in the pre-operative diagnosis of screen-detected breast carcinoma. Br J Cancer 2006;95:62-6.  Back to cited text no. 16
17.Bdour M, Hourani S, Mafleh W, Shabatat A, Karadsheh S, Nawaiseh O. Cytology of the breast: Comparism between fine needle aspiration cytology and tru-cut biopsy in the diagnosis of breast cancer. J Surg Pak 2008;13:19-21.  Back to cited text no. 17
18.Kocjan G. Needle aspiration cytology of the breast: Current perspective on the role in diagnosis and management. Acta Med Croatica 2008;62:391-401.  Back to cited text no. 18


  [Table 1], [Table 2], [Table 3]

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