Journal of Cytology
Home About us Ahead of print Instructions Submission Subscribe Advertise Contact e-Alerts Login 
Users Online:117
  Print this page  Email this page Small font sizeDefault font sizeIncrease font size


 
 Table of Contents    
ORIGINAL ARTICLE  
Year : 2022  |  Volume : 39  |  Issue : 4  |  Page : 159-162
Reproducibility of the “International academy of cytology yokohama system for reporting breast cytology” – A retrospective analysis of 70 cases


Department of Pathology, Burdwan Medical College, West Bengal University of Health Sciences, West Bengal, India

Click here for correspondence address and email

Date of Submission06-Nov-2021
Date of Decision13-May-2022
Date of Acceptance10-Oct-2022
Date of Web Publication28-Oct-2022
 

   Abstract 


Background: Fine-needle aspiration cytology (FNAC) is the most practiced initial method for evaluation of breast lesions. The International Academy of Cytology Yokohama System for Reporting Breast (IAC YSRB) Fine-Needle Aspiration Biopsy Cytopathology has been developed to standardize the reporting system. However, literature available on the inter-observer reproducibility of 5 IAC YSRB categories is limited. Aim: We investigated the inter-observer reproducibility of the IAC YSRB system. Method and Materials: A total of 70 consecutive specimens obtained from FNAC of breast lesions were reviewed retrospectively by 3 experienced cytopathologists who allotted 1 to 5 IAC YSRB categories. Results: The percent overall agreement between observers was 70.48% and the free marginal kappa was 0.63, which signifies substantial agreement. After combining “Suspicious” and “Malignant” categories, overall agreement was 80.95% and free marginal kappa became 0.75. Conclusions: Inter-observer agreement of three (70.48%) cytopathologists was substantial. Agreement can be improved by combining certain categories, especially “Suspicious” and “Malignant”. Technical quality limitation plays a significant role in a proportion of cases, mainly the “Atypical” and “Suspicious of malignancy” categories. Application of the IAC YSRB system in day-to-day practice will increase the inter-observer agreement.

Keywords: International Academy of Cytology Yokohama System, breast cytology, reproducibility

How to cite this article:
Boler AK, Roy S, Chakraborty A, Bandyopadhyay A. Reproducibility of the “International academy of cytology yokohama system for reporting breast cytology” – A retrospective analysis of 70 cases. J Cytol 2022;39:159-62

How to cite this URL:
Boler AK, Roy S, Chakraborty A, Bandyopadhyay A. Reproducibility of the “International academy of cytology yokohama system for reporting breast cytology” – A retrospective analysis of 70 cases. J Cytol [serial online] 2022 [cited 2022 Dec 6];39:159-62. Available from: https://www.jcytol.org/text.asp?2022/39/4/159/359793





   Introduction Top


Breast cancer is the most common cancer in women and is the leading cause of death in women aged 20–59 years. It accounts for 26% of all newly diagnosed cancer in females and is responsible for 15% of cancer-related deaths in females.[1] Initial evaluations for breast lesions include clinical and radiological examinations along with fine-needle aspiration cytology (FNAC). A number of guidelines have been developed to improve standardization of the terminology and criteria for cytological specimens obtained from the thyroid, pancreas, lungs, and salivary glands.[2] The International Academy of Cytology Yokohama System for Reporting Breast (IAC YSRB) recently developed a set of guidelines for reporting breast cytology. Five diagnostic categories were used in this IAC YSRB system to standardize breast cytology reporting. Each category is associated with a risk of malignancy (ROM) and management recommendation after FNAC. Diagnostic accuracy depends on a variety of factors, including clinical features[3],[4] and the skill of the cytopathologist in obtaining the cytologic materials.[5],[6],[7] However, very little information is available on the inter-observer reproducibility of five IAC YSRB categories. In this present study, 3 experienced cytopathologists examined and classified 70 consecutive cases according to the IAC YSRB categorical system to establish the inter-observer reproducibility.


   Materials and Methods Top


Since it was a retrospective study of specimens already collected and diagnosed, the study was exempt from approval by the Institutional Ethics Committee. The study population consisted of 70 consecutive FNAC samples of breast, performed over a period of one year (September 2020–June 2021). Out of the total patients, 69 were female and 1 was male. The age range was 17–60 years and all presented with palpable breast lesions. FNAC was performed using 22-gauge needle and a 10-ml syringe.[8] The cytology smears were stained by Papanicolaou stain, Haematoxylin and Eosin stain, and Leishman stain. Three experienced cytopathologists independently reviewed each slide and were unaware of the original diagnosis, clinical history, and image findings. Among the 3 cytopathologists, 1 had approximately 20 years of experience and the other 2 had 12 years and 8 years of experience, respectively. The cytopathologists each assigned the cases 1 to 5 diagnostic categories of the IAC YSRB system using the published criteria.[9] The inter-observer agreement was then established by statistical methods.

Statistical analysis

The guidelines for finding agreement among reviewers were followed using Fleiss' Kappa.[10],[11] Fleiss' Kappa is a generalization of Scott's pi statistic. It is a useful method for calculating inter-observer reliability.[12],[13],[14] Percent overall agreement statistics were performed with and without certain categories, to determine if agreement improved or deteriorated when different combinations of categories were made.


   Results Top


A total of 70 cases have been taken. An individual observer's diagnosis, as a percentage of the total number of cases, is in [Figure 1].
Figure 1: Individual observers' diagnosis, as a percentage of total number of cases (n = 70)

Click here to view


Percent overall agreement among three observers was 70.48% when interpretation was done according to original five IAC YSRB categories [Table 1]. The free marginal kappa was 0.63 which signifies substantial agreement.
Table 1: Overall agreements among observers

Click here to view


When category 4 (Suspicious) was merged with category 5 (Malignant), the percent overall agreement improved to 80.95%, and free marginal kappa value became 0.75 [Table 1].

Similarly, when category 2 (Benign) and category 3 (Atypical) were merged, the percent overall agreement improved to 78.10% and the free marginal kappa became 0.71 [Table 1].

However, when category 1 (Inadequate) and category 2 (Benign) were merged, there was no considerable improvement in agreement statistics [Table 1].

There were a total of 210 comparisons (3 observers × 70 cases). A concordant diagnosis was seen in the majority [132/210 (62.86%)]. Discordant diagnoses, like single category difference, were seen in 66/210 (31.43%) and three category difference was seen in 12/210 (5.71%) [Table 2].
Table 2: Summary of magnitude of discrepancies

Click here to view


The pairwise observed overall agreement between cytopathologists ranged from 67 to 72% and the pairwise kappa value ranged from 0.59 to 0.66 [Table 3].
Table 3: Pairwise observed agreement and kappa values

Click here to view


Thirty-two cases had a final histological diagnosis. Out of those, 19 cases had inter-observer disagreement [Table 4]. For the rest of the cases, follow-up data was retrieved from archive.
Table 4: Cases with inter-observer disagreement correlated with final histological diagnosis

Click here to view



   Discussion Top


Many guidelines have been proposed over the last decade aimed at producing definitions and diagnostic criteria that can be universally applied for reporting cytology specimens.

Some of these classification systems have gone one step further, toward providing an estimate of ROM for each of the proposed categories.[15],[16],[17] A major goal of these guidelines is to improve reproducibility and understanding of the reporting of diagnostic results among cytopathologists and between cytopathologists and clinicians.[2]

Therefore, in our study, we report the inter-observer reproducibility and their overall agreement, in line with the recently proposed IAC YSRB guidelines for breast cytology. Seventy consecutive cytology specimens obtained by FNAC of breast lesions were examined.

Inter-observer agreement among the observers was 70.48%. The majority of the discrepancy was seen between category 4 and category 5. When we merged category 4 and category 5, the percent overall agreement improved to 80.95%. This could be due to a lack of definite objective criteria between category 4 and category 5 of the IAC Yokohama system.

Of 70 cases, 32 cases had their final histological diagnosis. The majority of diagnostic disagreements were seen in low-grade carcinoma of no special type (NST), carcinoma with scanty material and in poorly stained smears. For example, in one case [shown in [Figure 2]a and [Figure 2]b] first observer rendered the diagnosis of category 4 due to low nuclear grade of the malignant cells. However, the other two observers rightly considered the lesion as category 5 as they stressed upon dispersal of cells, nuclear atypia (although mild), and occasional tubule formation. Another case of carcinoma NST (where malignant cells were mixed with benign cells and bare bipolar nuclei) was categorized as category 3 by the first two observers and category 4 by the third observer. This could be due to overshooting of the needle from the mass [Figure 2]c. Similar diagnostic discrepancies occurred in a case of low-grade ductal carcinoma due to the presence of cohesive papillary clusters, low nuclear grade, and occasional stripped nuclei [Figure 2]d. Three lobular carcinoma cases led to disagreement between observers due to low cellularity and mild nuclear atypia [Figure 3]. A single case of mucinous carcinoma was missed by all three observers due to the focal presence of scanty mucin and was diagnosed as fibroadenoma with prominent myxoid stroma [Figure 4]. The case of fat necrosis was reported as category 3 by one observer, which could be due to the presence of degenerated epithelial cells in the background [Figure 5].
Figure 2: Diagnostic discrepancy in infiltrating carcinoma NST: (a and b) This case of low grade carcinoma NST was missed by one observer due to cohesive fragments and mild nuclear atypia. (c) This case of carcinoma NST was missed by two observers due to the presence of admixed benign ductal epithelial cells (arrow) and bare nuclei, which could be due to overshooting of the needle from the mass. (d) This case was diagnosed as atypical by two observers due to presence of cohesive papillary clusters and occasional stripped nuclei. [Leishman stain, x40]

Click here to view
Figure 3:Diagnostic discrepancy in lobular carcinoma: (a and b) The left panel shows a case of lobular carcinoma diagnosed as atypical by two observers and benign by one observer. This error occurred due to mild nuclear atypia of the malignant cells. (Leishman stain, x40) (c and d) The right panel shows a case, which was diagnosed as atypical by first observer, insufficient/inadequate by second observer and benign by third observer. We believe the discrepancy occurred due to sampling issue. (Hematoxylin and Eosin stain, x40)

Click here to view
Figure 4: Diagnostic discrepancy in Mucinous carcinoma: (a–d) Due to the focal presence of scanty mucin, this case was diagnosed as fibroadenoma with prominent myxoid stroma by all three observers. (upper panel: Pap stain, x40; lower panel: Leishman stain, x40)

Click here to view
Figure 5: This case of fat necrosis was reported as atypical by one observer due to the presence of degenerated lipocytes in granular necrotic background. (Leishman stain, x 40) The lower left panel shows birefringent calcified necrotic fat under polarized light microscope

Click here to view


Thus, we can conclude that a few modifications could be made in the IAC Yokohama categories especially merging category 4 and category 5 that will increase inter-observer agreement. Technical quality limitation plays a significant role in a proportion of cases, especially in the “Atypical” and “Suspicious of malignancy” categories. However, application of the Yokohama system in reporting breast cytology cases in day-to-day practice will increase inter-observer agreement.

Acknowledgments

The authors are thankful to Dr. Goutam Banerjee, Dr. Rupam Karmakar, and Dr. Debasis Chakraborty for their help and support.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
De Wever O, Mareel M. Roll of tissue stroma in cancer cell invasion. J Pathol 2003;200:429-47.  Back to cited text no. 1
    
2.
Layfield LJ, Wang G, Yang ZJ, Gomez-Fernandez C, Esebua M, Schmidt RL. Intraobserver agreement for the international academy of cytology Yokohama system for reporting breast fine-needle aspiration biopsy cytopathology. Acta Cytol 2020;64:413-9.  Back to cited text no. 2
    
3.
Layfield LJ, Glasgow BJ, Cramer H, Fine-needle aspiration in the management of breast masses. In: Rosen PP, Fechner RE, editors. Pathology Annual. Part 2. Norwalk (CT): Apple-ton and Lange; 1989. p. 23-62.  Back to cited text no. 3
    
4.
Barrows GH, Anderson TJ, Lamb JL, Dixon JM. Fine-needle aspiration of breast cancer. Relationship of clinical factors to cytology results in 689 primary malignancies. Cancer 1986;58:1498-8.  Back to cited text no. 4
    
5.
Dixon GH, Lamb J, Anderson TJ. Fine needle aspiration of the breast: Importance of the operator. Lancet 1983;2:564.  Back to cited text no. 5
    
6.
Lee KR, Foster RS, Papillo JL. Fine needle aspiration of the breast. Importance of the aspirator. Acya Cytol 1986;31:281-4.  Back to cited text no. 6
    
7.
Boler AK, Banu N, Bose K, Roy S, Bandyopadhyay A. Reproducibility of “the Papanicolaou Society of Cytopathology system for reporting respiratory cytology”- A retrospective analysis of 101 cases of CT- guided FNAC. Diagn Cytopathol 2020;48:701-5.  Back to cited text no. 7
    
8.
Dey P. Diagnostic Cytology. 2nd ed. New Delhi: Jaypee; 2015. p. 210.  Back to cited text no. 8
    
9.
Field AS, Raymond WA, Rickard M, Arnold L, Brachtel EF, Chaiwun B, et al.; The International Academy of Cytology Yokohama System for Reporting Breast Fine-Needle Aspiration Biopsy Cytopathology. The international academy of cytology Yokohama system for reporting breast fine-needle aspiration biopsy cytopathology. Acta Cytol 2019;63 (Suppl. 4):257-7.  Back to cited text no. 9
    
10.
Fleiss JL. Measuring nominal scale agreement among many raters. Psychol Bull 1971;76:378-82.  Back to cited text no. 10
    
11.
Fleiss' Kappa-Statistics How To. Available from: https://www.statisticswto.datasciencecentral.com/Fleiss'Kappa. [Last accessed on 2019 Sep 23].  Back to cited text no. 11
    
12.
Nichols TR, Wisner PM, Cripe G, Gulabchnad L. Putting the kappa statistics to use. Qual Assur J 2010;13:57-61.  Back to cited text no. 12
    
13.
Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159-74.  Back to cited text no. 13
    
14.
Scott W. Reliability of content analysis: The case of nominal scale coding. Public Opin Quart 1955;17:321-5.  Back to cited text no. 14
    
15.
Baloch ZW, Livolsi VA, Asa SL, Rosai J, Merino MJ, Randolph G. Diagnostic terminology and morphologic criteria for cytological diagnosis of thyroid lesions: A synopsis of the National Cancer Institute. Thyroid fine-needle aspiration state of the science conference. Diagn Cytopathol 2008;36:425-37.  Back to cited text no. 15
    
16.
Layfield LJ, Baloch Z, editors. The Papanicolaou Society of Cytopathology System for Reporting Respiratory Cytology. 1st ed. Gewerbestrasse, Switzerland: Springer; 2019.  Back to cited text no. 16
    
17.
Pitman MB, Centeno BA, Ali SZ, Genevay M, Stelow E, Mino-Kenudson M. Standardized terminology and nomenclature for pancreatobiliary cytology: The Papanicolaou society of cytopathology guidelines. Diagn Cytopathol 2014;42:338-50.  Back to cited text no. 17
    

Top
Correspondence Address:
Dr. Arghya Bandyopadhyay
Department of Pathology, Burdwan Medical College, Burdwan – 713 104, West Bengal
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/joc.joc_203_21

Rights and Permissions


    Figures

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

  [Table 1], [Table 2], [Table 3], [Table 4]



 

Top
 
 
  Search
 
  
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Email Alert *
    Add to My List *
* Registration required (free)  


    Abstract
   Introduction
    Materials and Me...
   Results
   Discussion
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed554    
    Printed13    
    Emailed0    
    PDF Downloaded53    
    Comments [Add]    

Recommend this journal