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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 16  |  Issue : 2  |  Page : 334-339

International academy of cytology guidelines based categorization of breast fine-needle aspiration cytology lesions and their histopathological correlation


Department of Pathology, Mamata Medical College, Khammam, Telangana, India

Date of Submission17-Sep-2020
Date of Decision19-Dec-2020
Date of Acceptance08-Feb-2021
Date of Web Publication18-Oct-2021

Correspondence Address:
Dr. Shruti Amit Deshpande
Department of Pathology, Mamata Medical College, Rotary Nagar, Khammam - 507 002, Telangana
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jdmimsu.jdmimsu_335_20

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  Abstract 


Context: International academy of cytology (IAC) has established a standardized reporting system for fine-needle aspiration (FNA) cytology of breast lesions. They have introduced five categories (Code C1 to Code C5) for reporting breast cytology, each with clear descriptive term for the category, risk of malignancy (ROM) and a suggested management algorithm. Aim: Aims of the present study were to reclassify and correlate the breast FNA (IAC guidelines) with histopathological findings and to calculate the ROM for each category with special emphasis on assessing the diagnostic efficacy of cytological evaluation of code 3 and code 4. Materials and Methods: A 3 years' retrospective cross sectional study included 448 breast FNA samples that were reassessed and reclassified according to the IAC reporting system. The ROM for each category was analyzed. Results: The breast FNA samples were distributed in following categories as: C1 (insufficient material)− 1.78% (n = 8), C2 (benign) – 71.66% (n = 321), C3 (Atypical but benign) –10.81% (n = 45), C4 (Suspicious for malignancy) – 4.91% (n = 22), and C5 (Malignant)– 11.60% (n = 52). Out of the 448 cases, histopathological correlation was available for 205 cases. The ROM for each category was calculated as: 0% for C1, 2.04% for C2, 10.8% for C3, 85.71% for C4, and 100% for C5. The ability of C3 and C4 lesions to diagnose breast malignancy was statistically significant, P value 0.042 (P < 0.05). Conclusion: The IAC system for reporting of breast cytology effectively helps in accurate diagnosis and assessment of ROM for each category which helps in better patient management and further research.

Keywords: Breast lesions, fine-needle aspiration, international academy of cytology, risk of malignancy


How to cite this article:
Deshpande SA, Rao KS, Sushma Y, Saikumar GV. International academy of cytology guidelines based categorization of breast fine-needle aspiration cytology lesions and their histopathological correlation. J Datta Meghe Inst Med Sci Univ 2021;16:334-9

How to cite this URL:
Deshpande SA, Rao KS, Sushma Y, Saikumar GV. International academy of cytology guidelines based categorization of breast fine-needle aspiration cytology lesions and their histopathological correlation. J Datta Meghe Inst Med Sci Univ [serial online] 2021 [cited 2021 Nov 28];16:334-9. Available from: http://www.journaldmims.com/text.asp?2021/16/2/334/328469




  Introduction Top


Breast cancer has recently become the most common cancer in Indian women.[1] Triple assessment, which includes clinical, radiological, and fine-needle aspiration (FNA) cytology, has been an integral part for the evaluation of breast lesions. It ensures correct diagnosis and their precise treatment. Breast FNA remains one of the most important diagnostic modalities in developing countries due to lack of resources.[2],[3]

The international academy of cytology (IAC) in 2016 at Yokohama introduced a standardized system to categorize FNA breast lesions into five categories: Code 1 – code 5. The main goal of this system was to bring uniformity in reporting of the breast lesions. The assessment of risk of malignancy (ROM) for each category effectively stratify the breast lesions which provide management algorithm for the clinicians and facilitates the communication between cytopathologist and the clinical team for benefit of patient care and further research.[4]

Aims and objectives

  1. To reclassify the breast FNA according to IAC guidelines 2016 and correlate them with histopathological findings
  2. To calculate the ROM for each category with special emphasis on assessing the diagnostic efficacy of cytological evaluation of code 3 and code 4.



  Materials and Methods Top


The present study was conducted in the Department of Pathology, of a Tertiary Care Hospital from January 2017 to December 2019 after obtaining clearance from ethical committee. Total 448 cases were included in the study along with their relevant clinical and radiological data. All the FNA smears were reassessed and classified using the IAC Yokohama Reporting system for breast cytology into the following categories:

  • Code 1 (C1) – Insufficient material
  • Code 2 (C2) – Benign
  • Code 3 (C3) – Atypical probably benign
  • Code 4 (C4) – Suspicious, probably in situ or invasive carcinoma
  • Code 5 (C5) – Malignant.


Histopathological correlation was obtained in 205 cases.

Statistical analysis

The relevant data were entered into Microsoft Excel sheet and SPSS software (version 20, IBM Corporation, New York, USA), sensitivity, specificity, positive, and negative predictive values were calculated. The ROM was calculated for each category. ANOVA test was applied for code 3 and code 4. P < 0.05 was considered statistically significant.


  Results Top


In our study, the patients were distributed in a wide age group ranging from 13 years to 93 years. Most of the cases were in the second and third decades (54.68%). Out of the 448 cases 410 cases were females (91.52%) and males 38 (8.48%). Unilateral breast lesions 406 (90.62%) were predominantly noted. Right side breast lesions 211 (47.10%) cases were most common followed by left side 195 (43.52%) cases and bilateral 42 (9.38%) cases. Majority of the breast lumps were located in the upper outer quadrant 187 (41.75%). A wide range of size distribution varying from smallest (1 cm × 0.5 cm) to largest (10 cm × 8 cm) was observed. Nature of aspirate of all FNA samples were noted in which gray white aspirate was found in 148 cases (33.03%) followed by hemorrhagic mixed fluid in 112 cases (25%). Radiological investigations of all the cases were obtained and according to the BIRADS score, category 1 included two cases (0.45%), category 2–174 cases (38.84%), category 3–173 cases (38.62%), category 4–76 cases (16.95%), and category 5–23 cases (5.14%).

All the 448 FNA cases were reassessed and then categorized according to the IAC Reporting system. The distributions of the cases were C1 had eight cases (1.78%), C2-321 cases (71.66%), C3-45 cases (10.05%), C4-22 cases (4.91%), and C5-52 cases (11.60%) [Table 1].
Table 1: Correlation of international academy of cytology grading and histopathology with risk of malignancy for each category

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Among the C2 lesion, 123 (38.20%) cases were fibroadenoma followed by 110 (34.16%) cases of fibrocystic disease, 34 (10.56%) cases of gynecomastia, 11 (3.42%) cases of cystic lesion, eight (2.50%) cases of breast abscess, seven (2.17%) cases each of acute mastitis, galactocele and fibroadenoma with fibrocystic change. Five (1.55%) cases of inflammatory lesion, four (1.24%) cases of fat necrosis, three (0.93%) cases each of granulomatous mastitis and fibroadenoma with lactational changes were also observed [Table 2].
Table 2: Cytohistopathological distribution of breast lesions in C1 and C2 categories

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C3 lesions included 28 (62.22%) cases of benign proliferative breast disease with atypia, seven (15.57%) cases of fibroadenoma with atypia, five (11.11%) cases of papillary neoplasm, four (8.88%) cases of benign phyllodes tumor and one case of juvenile fibroadenoma (2.22%). C4 lesions included 22 cases of suspicious for malignancy [Table 3] and [Figure 1] and [Figure 2].
Table 3: Cytohistopathological correlation of breast lesions in categories C3 and C4

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Figure 1: (a and b) Cytosmears show benign ductal epithelial cells in clusters with mild nuclear atypia (H and E, ×40); Cytodiagnosis atypical but benign, category 3. (c) Histopathology shows features of atypical ductal hyperplasia (H and E, ×10)

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Figure 2: (a) Cytosmears showing clusters of atypical ductal epithelial cells with mild pleomorphism and hyperchromatic nuclei (H and E, ×40); Cytodiagnosis – suspicious of malignancy, category 4. (b) Histopathology shows features of Ductal Carcinoma In situ (H and E, ×40)

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C5 lesions included 38 (73.08%) cases of invasive ductal carcinoma-not otherwise specified (IDC-NOS), six (11.54%) cases of invasive lobular carcinoma (ILC), four (7.69%) cases of mucinous carcinoma, three (5.77%) cases of medullary carcinoma and one (1.92%) case of lymphoma [Table 4] and [Figure 3], [Figure 4], [Figure 5], [Figure 6].
Table 4: Cytohistological distribution of breast lesions in C5 category

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Figure 3: (a and b) Cytosmears show discohesive sheets of tumor cells with pleomorphic, hyperchromatic nuclei with prominent nucleoli (H and E, ×10 and × 40); Cytodiagnosis –Malignant, category 5. (c and d) Histopathology shows features of infiltrating ductal carcinoma (Grade II) (H and E, ×40)

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Figure 4: (a and b) Cytosmears show scattered atypical ductal epithelial cells against mucinous background (H and E, ×10 and × 40); Cytodiagnosis - malignant mucinous tumor, category 5. (c) Histopathology shows features of mucinous carcinoma (H and E, ×10)

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Figure 5: (a and b) Cytosmears show clusters atypical tumor cells admixed with lymphocytes and occasional giant cells in the background (H and E, ×40); Cytodiagnosis – medullary carcinoma, category 5. (c and d) Histopathology shows features of medullary carcinoma (H and E, ×40)

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Figure 6: (a) Cytosmear shows small, uniform tumor cells arranged in Indian file pattern (H and E, ×40); Cytodiagnosis – infiltrating lobular carcinoma, category 5. (b) Histopathology shows features of infiltrating lobular carcinoma (H and E, ×40)

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In our study, histopathological correlation was found in 205 cases and was considered as gold standard. In this, two cases of C1 category were diagnosed as benign breast disease (fibroadenoma and fibrocystic disease).

Among C2 lesions, histopathological correlation was available for 98 cases. Out of these, 96 were diagnosed as benign breast disease and two cases as malignant breast disease. Among the 96 cases, 66 cases were of fibroadenoma followed by 10 cases of fibrocystic disease, nine cases of gynecomastia and six cases of fibroadenoma with fibrocystic change. One case each of granulomatous mastitis, breast abscess, duct ectasia, galactocele, and keratinous cyst were diagnosed. The two malignant cases diagnosed histopathologically included IDC-NOS and malignant phyllodes tumor [Table 2].

In C3 category, histopathological correlation was available in 37 cases, in this 33 cases were diagnosed as benign breast disease and four cases were malignant. Among the 33 cases, seven cases were of atypical ductal hyperplasia (ADH), five cases of complex fibroadenoma, four cases benign phyllodes tumor, duct papilloma, tubular adenoma, and sclerosing adenosis. Two cases of usual ductal hyperplasia, one case each of juvenile fibroadenoma, adenomyoepithelioma, and fibroadenoma with apocrine metaplasia were diagnosed. Out of the four cases, two each of Ductal carcinoma in situ (DCIS) and IDC-NOS were diagnosed on histopathology [Table 3] and [Figure 1].

In C4 category, histopathological diagnosis was available in 21 cases, out of which 3 cases were benign breast disease and 18 turned out malignant. Two cases were diagnosed as ADH and one case as sclerosing adenosis on histopathology. Among the 18 malignant cases diagnosed histopathologically included 12 cases of IDC-NOS and six cases of DCIS [Table 3] and [Figure 2].

In C5 category, histopathological diagnosis was available in 47 cases. In this 35 cases were of IDC-NOS followed by six cases of ILC, four cases of mucinous carcinoma and two cases of medullary carcinoma [Table 4] and [Figure 3], [Figure 4], [Figure 5], [Figure 6].

The ROM for each category was calculated as 0% for C1, 2.04% for C2, 10.81% for C3, 85.71% for C4, and 100% for C5 [Table 1].

The P value (0.042) for the categories C3and C4 for diagnosing malignancy was significant at <0.05. The sensitivity, specificity, positive predictive value, and negative predictive values were determined as 95.58%, 95.62%, 91.54%, and 97.76%, respectively [Table 5].
Table 5: Sensitivity, specificity, positive predictive value and negative predictive value of breast of breast cytology

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  Discussion Top


Breast cancer is the most common cancer with high mortality rate worldwide. In India, it has overtaken cervical cancer with age adjusted incidence of 25.8/100,000 women population. Most of the breast lesions either present as benign or malignant.[1],[5],[6] Gray zone lesions coexist in between these two, which show significant overlap of the cytological features.[7] Various diagnostic modalities are available for diagnosing these lesions. In developed countries, core needle biopsy (CNB) has overtaken the FNA procedures. However, in developing countries, FNA still forms the most reliable and fundamental part of the triple assessment evaluation of breast lesions. Triple assessment assures accurate diagnosis of breast cancer in about 99% of the cases.

FNA procedure is a simple, rapid, noninvasive, cost-effective outpatient department procedure with minimum complication rate. Rapid on site evaluation and ultrasound-guided FNA procedures have reduced the rate of inadequate sampling and also improved the diagnostic efficacy of the test. FNA gives a clue about the benign and malignant lesions, but this differentiation is not possible in gray zone lesions. CNB is the most accurate test for diagnosis of such lesions. Although CNB has more advantages over FNA, it is more time consuming, invasive with higher rate of complications.[8],[9],[10],[11],[12],[13],[14],[15]

In 2016, the IAC at Yokohama formed the “Breast Group” which established a system for categorization of breast cytology reports into a five tier coding system (Code C1 – Code C5). This standardized reporting system was introduced with purpose of improving the training and performance of FNA, smear making and material handling techniques. It also aimed to improve the quality and reproducibility of the cytological reports. Thus it ensured a better communication with the clinicians in management of the patients and also enhances the use of ancillary tests for prognostic testing.[3]

The distribution of our samples according to IAC Yokohama system were comparable to the studies done by Panwar et al.,[16] Kamatar et al.,[17] Montezuma et al.,[18] Wong et al.,[19] and Hemalatha[20] [Table 6].
Table 6: Comparison between various studies done for international academy of cytology grading system

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In our study, 71 cases were diagnosed histopathologically as malignant lesions. Out of these two cases were cytologically diagnosed as benign. One case was cytologically diagnosed as fat necrosis but on histopathologically it was diagnosed as IDC-NOS. The cytological features in this case which favored the diagnosis of fat necrosis due to the presence of necrotic debris, inflammatory infiltrate, and occasional fragments of adipocytes. On histopathology, it was diagnosed as IDC-NOS. The second case was diagnosed as cystic lesion on cytology yielded only clear fluid on aspiration. On microscopic examination only cyst macrophages against proteinaceous background were seen, but on histopathology it was diagnosed as malignant phyllodes tumor. In both the cases, ultrasonography assisted FNA procedure was not conducted. In category C3, only 4 cases were diagnosed as malignant on histopathology. In category C4, 18 cases were histopathologically diagnosed as malignant. Three cases in category C4 which were suspicious for malignancy on cytology were diagnosed as benign proliferative breast disease with atypia on histopathology. None of the cases in category C 5 were diagnosed as benign on histopathology.

The ROM for each category was analyzed and compared with the previous studies done by Kamartar et al. and Montezuma et al. [Table 7].
Table 7: Comparison of risk of malignancy with previous studies

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Controversies have been reported for the specific diagnosis of the gray zone lesions. In the IAC reporting system debate has been widely focused on these lesions to be included in the categories C3 and C4 (gray zone).[3],[21],[22] In our study, the ability of diagnosing the malignant cases was more in C4 category compared to C3 category. Hence, it is recommended that further investigations such as CNB or trucut biopsy should be done in the gray zone lesions to arrive at accurate diagnosis.

Limitations

The main limitation of our study is lack of histopathological correlation in few atypical and malignant cases.


  Conclusion Top


The categorization of breast FNA cytology cases according to the IAC Yokohama system of reporting enhances the uniformity and quality assurance of the reports for better diagnosis and assessment of ROM in each category. It provides a better diagnostic clarity to the pathologist and guides the clinician for appropriate patient care.

Acknowledgment

The authors would like to thank the staff of Department of Pathology Mamata Medical College for the support and technical assistance.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Gupta S. Breast cancer: Indian experience, data, and evidence. South Asian J Cancer 2016;5:85-6.  Back to cited text no. 1
[PUBMED]  [Full text]  
2.
Hermansen C, Skovgaard Poulsen H, Jensen J, Langfeldt B, Steenskov V, Frederiksen P, et al. Diagnostic reliability of combined physical examination, mammography, and fine-needle puncture (”triple-test”) in breast tumors. A prospective study. Cancer 1987;60:1866-71.  Back to cited text no. 2
    
3.
Kachewar SS, Dongre SD. Role of triple test score in the evaluation of palpable breast lump. Indian J Med Paediatr Oncol 2015;36:123-7.  Back to cited text no. 3
[PUBMED]  [Full text]  
4.
Andrew SF, Fernando S, Philippe V. IAC Standardized reporting of breast fine-needle aspiration biopsy cytology. Acta Cytol 2017;61:3-6.  Back to cited text no. 4
    
5.
Malvia S, Bagadi SA, Dubey US, Saxena S. Epidemiology of breast cancer in Indian women. Asia Pac J Clin Oncol 2017;13:289-95.  Back to cited text no. 5
    
6.
Arul P, Masilamani S. Application of national cancer institute recommended terminology in breast cytology. J Cancer Res Ther 2017;13:91-6.  Back to cited text no. 6
    
7.
Nassar A. Core needle biopsy versus FNAB in breast: A historical perspective and opportunities in the modern era. Diagn Cytopathol 2011;39:380-8.  Back to cited text no. 7
    
8.
AL-Kaisi N. The spectrum of the “Gray Zone” in breast cytology. A review of 186 cases of atypical and suspicious cytology. Acta Cytol 1994;38:898-908.  Back to cited text no. 8
    
9.
Tikku G, Umap P. Comparative study of core needle biopsy and fine needle aspiration cytology in palpable breast lumps: Scenario in developing nations. Turk Patoloji Derg 2016;32:1-7.  Back to cited text no. 9
    
10.
Nguansangiam S, Jesdapatarakul S, Tangjitgamol S. Accuracy of fine needle aspiration cytology from breast masses in Thailand. Asian Pac J Cancer Prev 2009;10:623-6.  Back to cited text no. 10
    
11.
Field AS, Zarka MA. Breast. In: Field AS, Zarka MA, editors. Practical Cytopathology: A Diagnostic Approach to fine Needle Aspiration Biopsy. Amsterdam: Elsevier; 2017.  Back to cited text no. 11
    
12.
Joan C, Aylin S. Breast. In: Orell SR, Sterrett GF, editors. Fine Needle Aspiration Cytology. 5th ed. Toronto: Elsevier; 2012. p. 156-209.  Back to cited text no. 12
    
13.
Bajwa R, Tariq Z. Association of fine needle aspiration cytology with tumor size in palpable breast lesions. Biomedica 2010;26:124-9.  Back to cited text no. 13
    
14.
Kothari K, Tummidi S, Agnihotri M, Sathe P, Naik L. This 'rose' has no thorns—diagnostic utility of 'rapid on-site evaluation' (ROSE) in fine needle aspiration cytology. Indian J Surgl Oncol 2019;10:688-98.  Back to cited text no. 14
    
15.
Sunita H, Urmila T, Sharma DC. Cytomorphological study breast lesions with sonomammo-graphic correlation. J Evol Med Dent Sci 2015;4:137-42.  Back to cited text no. 15
    
16.
Panwar H, Ingle P, Santosh T, Singh V, Bugalia A, Hussain N. FNAC of breast lesions with special reference to IAC standardized reporting and comparative study of cytohistological grading of breast carcinoma. J Cytol 2020;37:34-9.  Back to cited text no. 16
[PUBMED]  [Full text]  
17.
Kamatar P, Athanikar V, Dinesh US. Breast fine needle aspiration biopsy cytology reporting using international academy of cytology Yokohama system- Two year retrospective study in tertiary care centre in Southern India. Natl J Lab Med 2019;8:001-3.  Back to cited text no. 17
    
18.
Montezuma D, Malheiros D, Schmitt FC. Breast fine needle aspiration biopsy cytology using the newly proposed IAC Yokohama system for reporting breast cytopathology: The experience of a single institution. Acta Cytol 2019;63(suppl-4):274-79.  Back to cited text no. 18
    
19.
Wong S, Rickard M, Earls P, Arnold L, Bako B, Field AS, et al. The international academy of cytology Yokohama system for reporting breast fine needle aspiration biopsy cytopathology: A single institutional retrospective study of the application of the system categories and the impact of rapid onsite evaluation. Acta Cytol 2019;63:280-91.  Back to cited text no. 19
    
20.
Hemalatha A, Prasad CS. Correlation of fine needle aspiration of breast lesions (IAC categories) with histopathology and emphasis on code 3 and 4. J Clin Biomed Sci 2018;8:80-4.  Back to cited text no. 20
    
21.
Kanhoush R, Jorda M, Gomez-Fernandez C, Wang H, Mirzabeigi M, Ghorab Z, et al. 'Atypical' and 'suspicious' diagnoses in breast aspiration cytology. Cancer 2004;102:164-7.  Back to cited text no. 21
    
22.
Mendoza P, Lacambra M, Tan PH, Tse GM. Fine needle aspiration cytology of the breast: The nonmalignant categories. Patholog Res Int 2011;2011:547580.  Back to cited text no. 22
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]



 

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