
==== Front
J Cytol
J Cytol
JCytol
J Cytol
Journal of Cytology
0970-9371
0974-5165
Wolters Kluwer - Medknow India

JCytol-41-162
10.4103/joc.joc_167_22
Original Article
Effectivity of Touch Imprint Cytology of Core Needle Biopsy in Evaluation of Breast Lesions: A Study in Changing Trends of Rapid on Site Evaluation
Boler Anup Kumar
Roy Shreosee
Singh Ph Priyanca
Maiti Barnali
Department of Pathology, Burdwan Medical College, Burdwan, West Bengal, India
Address for correspondence: Dr. Barnali Maiti, Tikarhat, P.O- Lakurdi, Burdwan - 713 102, West Bengal, India. E-mail: barnali.bmc@gmail.com
Jul-Sep 2024
18 7 2024
41 3 162165
03 12 2022
16 3 2024
03 6 2024
Copyright: © 2024 Journal of Cytology | Indian Academy of Cytologists
2024
https://creativecommons.org/licenses/by-nc-sa/4.0/ This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.
Background:

Touch imprint cytology (TIC) of core needle biopsy specimen is an easy method of rapid on-site evaluation (ROSE) which aids in the rapid diagnosis of breast lumps by cytological analysis.

Objective:

To evaluate the efficacy of touch imprint cytology in predicting the adequacy of needle core biopsy of breast lumps and its diagnostic accuracy for malignancy.

Materials and Methods:

This study was done in Burdwan Medical College over a period of two years on 80 patients who had presented with breast lumps and had given consent for core needle biopsy for diagnosis.

Results:

Out of 80 cases, satisfactory materials on touch imprint were obtained in 79 cases. Only one case did not yield satisfactory material and hence was excluded from the analysis. A total of 43 cases were malignant, and 36 cases were either benign or inflammatory on core needle biopsy. Thirty-seven cases were accurately diagnosed as malignant by TIC, and 35 cases were accurately diagnosed as benign by TIC. Sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of TIC were 86.05%, 97.22%, 97.37%, and 85.36%, respectively, and the overall accuracy was 90%.

Conclusion:

TIC of core needle biopsy is a rapid, reliable, and accurate method for early cytological diagnosis of symptomatic breast lesions. It can be used routinely at the site of biopsy to evaluate the adequacy of materials obtained during core needle biopsy and to plan for further workup in case of malignant breast lesions.

Core needle biopsy
ROSE
touch imprint
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pmcINTRODUCTION

Breast cancer has emerged as the commonest cancer among women in the developed as well as developing countries worldwide.[1] Evaluation of breast lumps includes clinical examination, imaging (mammography), and fine needle aspiration cytology and/or core needle biopsy, collectively known as triple assessment. In the era of personalized medicine, cytopathologists need to make not only rapid but also accurate diagnosis. Hence, the evaluation of touch imprint cytology (TIC) of core needle biopsies (CNB) has become more relevant than rapid on-site evaluations (ROSE) performed on fine-needle aspiration.[2]

CNB provides histomorphological interpretation that includes information about tumor type, grade, and lympho-vascular invasion. It also provides platform for immunohistochemistry-based assessment of prognostic and predictive markers, thereby helping in the therapeutic strategy before operation.

TIC of core needle biopsy specimen is a very easy technique for rapid evaluation of sample adequacy which can be done quickly in the same sitting.

In this study, our aim was to evaluate the effectivity of touch imprint cytology in predicting the adequacy of core needle biopsy of breast lumps and its diagnostic accuracy in detecting pathology specially malignancy.

MATERIALS AND METHODS

The study was conducted in the Department of Pathology, Burdwan Medical College, for two consecutive years from July 2020 to June 2022. The study was conducted after obtaining informed consent from all patients presenting with palpable breast lumps in cases where FNAC and mammographic findings were suspicious including those which produced equivocal results. CNBs were taken by 16-gauge needle, aseptically under local anesthesia with 2% xylocaine/lignocaine solution. In all the cases, touch imprints were obtained by gently rolling the fresh unfixed tissue to clean glass slides. At least three imprint smears were made in each case avoiding blood and mucus. One of the smears was air-dried, and one was immediately fixed in ultrapap spray fixative. The air-dried smears were stained with Leishman–Geimsa (LG) stain, and the alcohol fixed smears were stained with Papanicolaou (Pap) by Ultrapap methods. The third slide was used for any special stain like Zeihl Neelsen (ZN) Stain for acid–fast bacilli or Periodic acid–Schiff (PAS) for fungus in suspected cases or kept unstained. The tissue was then put in 10% neutral buffer formalin and submitted for routine histopathological study. All the slides were assessed for sample adequacy. The degree of diagnostic accuracy was done by comparing them with their corresponding histopathological sections subsequently.

We followed The International Academy of Cytology (IAC) Yokohama System for Reporting Breast Fine Needle Aspiration Biopsy Cytopathology for adequacy criteria of imprint smears in this study. The adequacy criteria were applicable for parenchymatous lesions which required approximately 6–7 epithelial tissue fragments (clusters), each consisting of at least 10–20 cells (so that the architecture of the tissue fragments and the presence or absence of myoepithelial cells can be assessed)[34] or any number of appropriately smeared and fixed epithelial cells.[567]

A diagnosis of malignancy on TIC was considered as true positive if the final diagnosis on biopsy (CNB) evaluation was positive for malignancy. Similarly, a diagnosis of benign lesion on TIC was considered true negative if the final diagnosis was benign on biopsy. A diagnosis of malignancy given on TIC if it was found to be benign on biopsy was considered as false positive. A diagnosis of benign lesion on TIC if it was found to be malignant on biopsy considered to be false negative. Based on these findings, the overall sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of TIC diagnosis were evaluated.

RESULT

A total of 80 cases of breast lumps including one male patient were studied. The age of the patients ranged from 20 to 71 years with a mean of 43.70 yrs. The most common age group having breast lumps in sample population was patients of fifth decade. Adequate and satisfactory material on touch imprint was obtained in 79 (98.75%) cases.

All the TIC smears were examined and categorized into insufficient/inadequate, benign, atypical, suspicious of malignancy, and malignant entities, under IAC Yokohama System for Reporting Breast Fine Needle Aspiration Biopsy Cytopathology [Table 1]. Thirty-seven benign and 43 malignant cases were diagnosed on CNB [Table 2].

Table 1 Lists of diagnoses obtained by TIC

Diagnosis on TIC	IAC Yokohama reporting system	No of cases	Percentage (%)	
Abscess, Organizing, and granulomatous inflammation	Benign	12	15.00	
Fibroadenoma	Benign	09	11.25	
Fibroadenoma with atypia	Atypical	01	1.25	
Fibrocystic disease	Benign	12	15.00	
Proliferative breast disease	Benign	04	5.00	
Proliferative breast disease with atypia	Atypical	04	5.00	
Suspicious for malignancy	Suspicious of malignancy	03	3.75	
Malignant (no exact categorization)	Malignant	34	42.5	
Inadequate For Evaluation	Insufficient/inadequate	01	1.25	
Total No of cases		80	100	

Table 2 Comparison of diagnoses obtained by TIC with corresponding CNB

Diagnosis on TIC	No of Cases	Diagnosis on CNB	
Inflammatory	12	Abscess (02), granulomatous mastitis (04), tubercular mastitis (02), Organizing breast abscess (02), lymphocytic mastopathy (1), benign breast disease with fat necrosis (1)	
Fibroadenoma	11	Fibroadenoma (7), fibroadenoma with atypia (1), fibroadenoma with focal epitheliosis (1), phyllodes (2)	
Fibrocystic disease and fibroadenosis	10	Fibroadenosis (5), fibrocystic disease of breast (3), fibroadenosis with small focus of invasive carcinoma (1), Secretory carcinoma (1)	
Proliferative breast disease	04	Phyllodes tumor (2), fibrocystic disease with usual ductal hyperplasia (1), invasive (ductal) carcinoma, NST, grade 1 (1)	
Proliferative breast disease with atypia	04	Lobular carcinoma of breast (1), invasive (ductal) carcinoma, NST, grade 1 (1), high grade DCIS with small focus of invasion (1), blunt duct adenosis with CAPSS, and flat epithelial atypia (1)	
Suspicious for malignancy	04	Fungal granulomatous mastitis (1), invasive (ductal) carcinoma, NST, grade 1 (2), invasive (ductal) carcinoma, NST, grade 2 (1)	
Malignant (no exact categorization)	34	Invasive (ductal) carcinoma, NST, grade 1 (4), invasive (ductal) carcinoma, NST, grade 2 (13), invasive (ductal) carcinoma, NST, grade 3 (15), invasive (ductal) carcinoma with extensive ductal carcinoma in situ (DCIS) component (2)	
Inadequate For evaluation	01	Fibrocystic disease of breast (1)	

Out of 37 benign cases as per HPE, one TIC smear was inadequate for evaluation. Thirty-five cases were correctly diagnosed as benign (true negative-TN), and 1 false positive (FP) was diagnosed as suspicious for malignancy on TIC [Table 3].

Table 3 Two-by-two contingency table

Cases (Tissue Diagnosis)	Malignant (TIC Diagnosis)	Benign (TIC Diagnosis)	
Malignant (n-43)	37 (TP)	06 (FN)	
Benign (n-36)	01 (FP)	35 (TN)	

Whereas out of 43 malignant cases as per HPE, 37 cases were found malignant and suspicious for malignancy (true positive-TP) with six false negative (FN) benign findings on TIC [Table 3].

Sensitivity of TIC = 86.05%, specificity = 97.22%, positive predictive value (PPV) =97.37%

Negative predictive value (NPV) =85.36%

Overall accuracy = (100%- %of error) =90%

DISCUSSION

Dudgeon and Patrick first described TIC for diagnosis of cancer in 1927.[8] Subsequently, in many studies, TIC was found to be useful not only for the evaluation of sentinel node in breast cancer[9] and mucosal cut margins in oral cancer[10] but also as an aid to intraoperative frozen section.[11] In the current study, we evaluated 80 cases of breast lumps and undergone CNB and TIC. We used dual stains which included LG and rapid Pap (for every case). The stains are complementary to each other as LG brings out the cytoplasmic character of cells, whereas alcohol fixed pap stain brings out the nuclear character better. It was not possible to form any conclusive opinion in one case of TIC due to cellular paucity and crushing artifacts. However, core needle biopsy of this case was satisfactory and benign in diagnosis. Rest 79 cases of TIC were adequate for evaluation, thus assessing the adequacy of core biopsy.

We could categories the benign and nonneoplastic lesions on TIC. Numerous neutrophils in abscess, granulomas, and chronic inflammatory cells in granulomatous mastitis, caseating granulomas with Langhans giant cells along with ZN stain positivity for acid–fast bacilli in tuberculous mastitis were well appreciated in the TIC smears. Benign breast diseases were identified by cohesive clusters of uniform epithelial cells in background of bare bipolar nuclei. Smears were marked as atypical when benign features were superadded with some uncommon features like prominent single intact cell dispersal, nuclear enlargement and pleomorphism, high cellularity, necrosis, mucin and complex micropapillary, and cribriform architectural features. TIC smears of suspicious for malignant cases showed malignant cellular features which are less than sufficient in quality or quantity. High cellular yield of discohesive clusters with nuclear pleomorphism, hyperchromasia, prominence of nucleolus, and dispersed single intact cells unequivocally categorized the smear as malignant [Figures 1 and 2].

Figure 1 (a) Discohesive cell clusters with prominent anisonucleosis and nuclear hyperchromasia LG 40×; (b) nuclear pleomorphism and brisk mitotic activity CNB HE 40×

Figure 2 (a) Cellular smear showing tubule formation LG 40×; (b) Grade 1 IDC with DCIS component CNB HE 10×; (c) Invasive and In situ component HE 40×

In the present study, we found one false-positive case and six false-negative cases. Final biopsy evaluation of the false-positive case showed fungal mastitis with reactive changes in ductal epithelial cells. Subsequent PAS stain on TIC revealed fungal elements. The six false-negative cases included two cases of grade 1 invasive ductal carcinoma, one each of high-grade DCIS with small focus of invasion, fibro adenosis with small focus of invasive carcinoma, secretory carcinoma, and lobular carcinoma of breast. Most of them showed small foci of grade 1 invasive carcinoma within mostly desmoplastic stroma with admixture of benign components on biopsy. Lobular carcinoma of breast showed low cellularity and low nuclear grade which was interpreted as atypical on ROSE [Figure 3]. TIC of secretory carcinoma had low cellularity with low N: C ratio in the background of proteinaceous secretory material with associated benign components [Figure 4].

Figure 3 (a) Small rounded cells in small discohesive clusters LG 40×; (b) Indian file pattern in HE 10×; (c) Lobular carcinoma HE 40×

Figure 4 (a) Benign looking cells in small groups LG 40×; (b) Microcystic, tubular and solid architecture, HE 10×; (c) Low grade cytologic atypia, vacuolated cytoplasm, and apical snouts HE, 40×

In the present study, the sensitivity of TIC was found to be 86.05%, the value of which is slightly lower in comparison to previous studies done by of Kulkarni D et al., 2009,[12] and Kehl et al.,[13] and Sivaprasad S et al., 2017.[14] This was due to the presence of low-grade breast cancer, presence of only in situ component, and presence of tiny foci of invasive cancer in background of fibroadenosis that created confusion in TIC.

The specificity (97.22%), positive predictive value (97.37%), negative predictive value (85.36%), and overall accuracy (90%) were well correlated with the said studies.

To conclude, TIC is a very rapid, easy, and reliable technique for evaluation of adequacy of biopsy material required for early diagnosis and ancillary investigations. Routine use of TIC is therefore essential in CNB-based diagnostic workup for suspected malignant breast pathology. Adequacy criteria of IAC Yokohama System for Reporting Breast Fine Needle Aspiration Biopsy Cytopathology satisfy the same for TIC as well. The quick result also helps in deciding further surgical management or preoperative neoadjuvant chemo/radiotherapy.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.
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