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Year : 2020  |  Volume : 63  |  Issue : 4  |  Page : 581-586
Utility of cell block as an adjunct to liquid-based cytology for diagnosing papillary thyroid carcinoma

1 Department of Pathology and Laboratory Medicine, Taichung Veterans General Hospital, Taichung, Taiwan
2 Department of Pathology and Laboratory Medicine, Taichung Veterans General Hospital; Department of Medical Laboratory Science and Biotechnology, Central Taiwan University of Science and Technology, Taichung, Taiwan

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Date of Submission23-Dec-2019
Date of Decision07-Apr-2020
Date of Acceptance22-Apr-2020
Date of Web Publication28-Oct-2020


Background: Although liquid-based cytology (LBC) has gained popularity among clinical laboratories, it is unclear whether it is equivalent to conventional smears for making a definite diagnosis of papillary thyroid carcinoma (PTC). The Bethesda System for Reporting Thyroid Cytopathology (TBSRTC) suggests a definite diagnosis of PTC is preferred when there are at least one of three features (papillary architecture, psammomatous calcifications, and frequent pseudonuclear inclusions) plus other typical cytomorphological findings. This study evaluated whether an additional cell block (CB), prepared from the residual LBC material, could help improve the diagnosis of PTC. Materials and Methods: A total of 62 cases with both ThinPrep LBC and CB preparations and histopathological follow-up of PTC were retrieved between November 2016 and March 2019. The ThinPrep LBC and CB slides were reviewed separately to identify any papillary architecture, psammomatous calcifications, or pseudonuclear inclusions for diagnosing PTC. Results: Among the 51 cases with cytological diagnosis of PTC in the LBC+CB slides, the CB provided additional diagnostic information in 15 cases, which were initially diagnosed as suspicious for PTC based on the LBC slides alone. This information included papillary architecture (n=11), psammomatous calcification (n=1) and pseudonuclear inclusions (n=5). The number of specimens in the 51 cases containing at least one of the three features increased from 42 (LBC) to 51 (LBC+CB). The accuracy for diagnosing PTC increased from 58.1% for LBC alone to 82.3% for the LBC+CB examination. Conclusion: An adjunctive CB preparation may improve the LBC technique for diagnosing PTC.

Keywords: Cell block, liquid-based cytology, papillary thyroid carcinoma, The Bethesda System for Reporting Thyroid Cytopathology

How to cite this article:
Chen YA, Lai YC, Lin SJ, Yang CS. Utility of cell block as an adjunct to liquid-based cytology for diagnosing papillary thyroid carcinoma. Indian J Pathol Microbiol 2020;63:581-6

How to cite this URL:
Chen YA, Lai YC, Lin SJ, Yang CS. Utility of cell block as an adjunct to liquid-based cytology for diagnosing papillary thyroid carcinoma. Indian J Pathol Microbiol [serial online] 2020 [cited 2020 Nov 25];63:581-6. Available from: https://www.ijpmonline.org/text.asp?2020/63/4/581/299340

   Introduction Top

Fine needle aspiration (FNA) cytology is a cost-effective, simple, and useful method for evaluating thyroid nodules. Conventional smears (CS) are an established preparation technique for managing FNA specimens, and cytopathologists are familiar with the cytomorphological features of thyroid lesions, especially papillary thyroid carcinoma (PTC).[1] Thus, CS-based techniques have been considered effective for diagnosing thyroid lesions. However, liquid-based cytology (LBC) is an emerging technique that has recently become popular among clinical laboratories for managing FNA biopsy of thyroid lesions, as it provides simple specimen collection and processing, as well as excellent cell preservation.[2],[3] Despite the success of LBC-only approach as an alternative to CS method as demonstrated in some large academic institutes, controversy remains regarding its efficacy and diagnostic accuracy when it is used alone. The main concern is that the LBC-alone approach fails to improve the definite diagnostic rate for PTC, relative to CS.[4],[5],[6],[7] Moreover, PTC may be initially underdiagnosed by cytopathologists and cytologists when the laboratory converts from CS to LBC, given their unfamiliarity with the alterations of cell cluster architecture and nuclear features. For example, papillary architecture and large tissue fragments are reduced in LBC, and intranuclear pseudoinclusions are smaller and less obvious in LBC than in CS.[8],[9]

A definite diagnosis of PTC based on FNA cytology requires a constellation of characteristic cytological features, including nuclear enlargement and molding, powdery chromatin, nuclear grooves, pseudonuclear inclusions, nuclear membrane irregularity, papillary structure, and psammomatous calcification. However, none of these features is entirely specific.[10] According to the suggestions in the Bethesda System for Reporting Thyroid Cytopathology (TBSRTC), a definite diagnosis of PTC could be rendered when the specimens contains at least one of three following features (i.e., papillary structure, frequent pseudonuclear inclusions, and psammomatous calcifications) along with other typical cytomorphological features.[11] Therefore, this study aimed to identify these three features using ThinPrep LBC and cell block (CB) slides prepared from the residual LBC material, in order to verify whether the combined use of LBC and CB could improve the diagnosis of PTC, relative to the LBC-alone approach.

   Materials and Methods Top

The retrospective study protocol was approved by the institutional review board of the hospital (CE19156A). We searched our cytopathology archives to identify thyroid FNA cytology reports that were collected between November 2016 and March 2019. During this period, 124 specimens handled by the department had a cytological diagnosis of either suspicious for papillary thyroid carcinoma (SPC) or PTC. Ninety-eight cases had both ThinPrep and CB preparations, with surgical follow-up available in 62 of these cases. Thyroid FNA was performed under ultrasound guidance by experienced endocrinologists and otolaryngologists, but without rapid on-site evaluation. The aspirates had been collected in CytoLyt solution, and the Papanicolaou-stained LBC slides were prepared using a ThinPrep 5000 automated slide processor (Hologic; Marlborough, MA, USA) according to the manufacturer's instructions. One ThinPrep slide was prepared for each specimen, and a CB had been prepared according to the Histogel method when residual LBC material was available. The CB sections were processed according to our standard histology protocols and stained with hematoxylin and eosin.

The LBC and CB slides of the 62 cases were re-evaluated by one cytotechnologist and two pathologists in the department. In each case, an initial diagnosis was determined by LBC alone and then a final diagnosis was made with the combination of LBC and CB. The LBC and CB slides were independently reviewed by two of the authors (Y.-A.C. and C.-S.Y.) to identify any instances of papillary architecture, psammomatous calcifications, or frequent pseudonuclear inclusions. Papillary architecture was defined as a true papillary tissue fragment that exhibited a fibrovascular core lined by neoplastic cells, or crowded papillary structures with a three-dimensional configuration. Frequent pseudonuclear inclusions were defined as the presence of three or more inclusions in one slide. In each case, the presence of these features described above was documented as in LBC, CB, and LBC+CB.

McNemar's test was used to evaluate the cytological features of PTC between the three sample groups (LBC alone, CB alone, and LBC+CB). Differences were considered statistically significant at P values of <0.05. All statistical analyses were performed using IBM SPSS software program, version 22.0 (IBM, Armonk, New York).

   Results Top

During the study period, we identified 124 thyroid FNA specimens, including 62 specimens with both corresponding CB preparations and surgical follow-up via lobectomy or thyroidectomy. All of the histopathological diagnoses were PTC. The FNA specimens were taken from 62 patients (51 women, 11 men) with an average age of 46.7 years (range: 21–65 years). An adequate CB preparation was achieved for 47 specimens, while the CB slides for 15 specimens were considered inadequate because of scarce or absent lesion cells. All 62 cases were classified into PTC (n=36) and SPC (n=26) based on LBC alone. With addition of the CB, 15 cases with initial diagnosis of SPC were reclassified as PTC. The accuracy for diagnosing PTC increased from 58.1% for LBC alone to 82.3% for the LBC+CB examination.

Among the 62 specimens, higher cellularity was found in CB than in LBC in 7 specimens. The total numbers of the papillary architecture, psammomatous calcifications and pseudonuclear inclusions in LBC, CB and LBC+CB slides of the 51 specimens with cytological diagnosis of PTC are listed in [Table 1] and [Table 2]. No significant differences were observed when we compared the LBC and CB slides in terms of papillary architecture (P = 0.556) and psammomatous calcification (P = 1.000), although a significant difference was observed for pseudonuclear inclusions (P = 0.017). No significant difference was observed between the LBC and CB slides when we considered the presence of one or more of these features (P = 0.170), though a significant difference was observed when we compared LBC+CB to LBC alone (P = 0.004). Comparison of single features between LBC+CB and LBC alone revealed significant difference in papillary architecture (P < 0.001), but not psammomatous calcification (P = 0.250) and pseudonuclear inclusions (P = 0.063). Relative to the LBC slides alone, inclusion of the CB slides which helped to change the diagnosis from SPC to PTC in 15 cases [Table 3] revealed additional cytological features associated with PTC, including papillary architecture (n = 11), psammomatous calcification (n = 1), and pseudonuclear inclusions (n = 5) [Figure 1] and [Figure 2]. Of the 11 cases with the diagnosis of SPC in the combined use of LBC and CB specimens [Table 4], CB had minimal effect in the assistance of diagnosing of PTC. There were 4 inadequate specimens and only one additional cytological feature (psammomatous calcification) associated with PTC was present [Figure 3].
Table 1: Comparison between LBC and CB of the 51 cases with the diagnosis of PTC

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Table 2: Comparison between LBC and LBC+CB of the 51 cases with the diagnosis of PTC

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Table 3: Comparison between LBC and LBC+CB of the 15 cases with reclassification of the diagnosis from SPC to PTC

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Figure 1: (a) A small tissue fragment with an admixture of abundant foamy histiocytes (Papanicolaou stain, ×100). (b) The epithelial cells exhibit oval or irregular-shaped nuclei, marginally placed eosinophilic nucleoli, and vacuolated cytoplasm. An inconspicuous pseudonuclear inclusion (arrow) is observed (Papanicolaou stain, ×400). (c) The corresponding cell block exhibits large complex papillary tissue fragments(hematoxylin and eosin, ×100). (d) The histological follow-up reveals a cystic variant of papillary thyroid carcinoma (hematoxylin and eosin, ×20)

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Figure 2: (a) The monolayer sheet consists of cells with ovoid to irregular-shaped and raisin-like nuclei with focal molding (Papanicolaou stain, ×400)(b and c) The corresponding cell block exhibits microfollicular structures with psammomatous calcification (hematoxylin and eosin, ×200). (d) The subsequent histology of papillary thyroid carcinoma shares morphology and architecture similar to those of the cell block (hematoxylin and eosin, ×100)

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Table 4: Comparison between LBC and LBC+CB of the 11 cases with the diagnosis of SPC

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Figure 3: (a and b) The syncytial tissue fragments are composed of histiocytoid epithelial cells with scalloped border containing enlarged and pale nuclei with dense to vacuolated cytoplasm (Papanicolaou stain, ×400). (c) Psammoma body formation (arrow) lined by tumour cells is observed in the corresponding cell block (hematoxylin and eosin, ×400). (d) The surgical follow-up reveals papillary thyroid carcinoma with psammomatous calcification (hematoxylin and eosin, ×200)

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   Discussion Top

Liquid-based preparations have been widely used for managing cytopathological specimens in recent years. Relative to CS, LBC provides optimal cell preservation with fewer air-drying artefacts, fewer slides, shorter screening time, easier technical preparation, and a cleaner background because there is decreased obscuring material. Moreover, CB slides prepared from the well-preserved cellular remnants of LBC specimens could be used for further histopathological examination, immunohistochemical analysis, and molecular testing.[6],[12]

Despite the advantages of LBC over CS, there remain conflicting opinions regarding the diagnostic utility of LBC alone for evaluating thyroid FNA specimens.[5],[6],[7] For example, Biscotti et al.,[2] Rossi et al.,[4] and Scurry et al.[13] reported that LBC was as effective as CS when the LBC slides were reviewed by experienced cytopathologists. However, Frost et al.,[14] Cochand-Priollet et al.,[15] and Lee et al.[16] have reported that CS provides a lower non-diagnostic rate and a higher proportion of definite malignant diagnosis, relative to LBC preparations. Fischer et al.[17] analyzed 47,076 responses for thyroid FNA from the College of American Pathologists Interlaboratory Comparison Program in Non-Gynecologic Cytology, and reported that, among slides with a reference diagnosis of PTC, the diagnostic accuracy was 87.3% for CS and 82.3% for LBC. The difference between the two preparations in the diagnostic efficacy of papillary carcinoma may be mainly due to the morphologic changes inherent to LBC during the specimen processing. Michael and Hunter[9] compared the cytomorphological difference of 120 FNA specimens, including 13 thyroid gland tissues, that were simultaneously prepared using CS and ThinPrep, and reported that some architectural and cellular alterations were created by the ThinPrep technique. For example, large branching sheets and papillary structures tended to break into smaller clusters and were accompanied by the presence of more single cells. In addition, the ThinPrep cells were generally smaller and had more obvious nucleoli than the CS cells, and the pseudonuclear inclusions were less evident and more difficult to identify in the ThinPrep slide. Suzuki et al.[8] have also reported that, relative to CS, the cytological features of PTC frequently observed in LBC were trabecular and hobnail patterns, convoluted nuclei, eosinophilic nucleoli, and a perinucleolar halo, with fewer papillary structures, less tissue fragments, and inconspicuous pale nuclei.

In this study, the CB slides only exhibited higher cellularity than the ThinPrep slides in 11.3% of the specimens (n = 7), and 24.2% of the CB slides (n = 15) were considered inadequate due to scarce or absent cellularity. These findings agree with previous reports that ThinPrep slides can exhibit greater cellularity and provide a higher diagnostic yield than CB slides.[18],[19] Nevertheless, 24.2% of the cases (n = 15) were reclassified as PTC from SPC with the assistance of CB slides, which offered some additional diagnostic information associated PTC including papillary architecture (n = 11), psammomatous calcification n = 1), and pseudonuclear inclusions (n = 5). Moreover, the morphology of the papillary architecture was different in ThinPrep slides from that in CB slides. The papillary architecture in the ThinPrep slides frequently exhibited small papilla with a fibrovascular core, rather than a three-dimensional configuration, which sometimes needed to be scrutinized more carefully, while the CB slides tended to exhibit a large complex architecture [Figure 4]. When we compared the LBC+CB results to the LBC-alone results in the 51 cases with diagnosis of PTC, the combination provided significantly larger proportions of cases with papillary structure (74.5% vs. 45.1%, P<0.001). Furthermore, the number of specimens in which the presence of at least one of the three features increased from 42 (LBC) to 51 (LBC+CB). Our results demonstrated that combining LBC and CB preparations had improved the diagnostic accuracy to 82.3% from 58.1% as in the LBC-only approach.
Figure 4: (a) The papillary pattern of conventional papillary thyroid carcinoma in the ThinPrep slides involves small papilla with a central fibrovascular core. (b) The corresponding cell block shows mostly large and complex papillary architecture (hematoxylin and eosin, ×40)

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Near-total or total thyroidectomy with elective lymph node sampling for potential metastasis is the standard treatment strategy for patients with a cytological diagnosis of PTC. However, a two-stage procedure may be required in the absence of a definite diagnosis, which involves initial lobectomy with an intraoperative frozen section or imprint cytology to confirm the diagnosis and determine if removal of residual thyroid tissue is necessary.[6],[10],[17] Our study suggested that, in cases with a diagnosis of SPC based on the initial ThinPrep slide, an additional CB preparation would probably improve the treatment selection for thyroid neoplasms.

A CB preparation is considered a reliable complementary method for evaluating cytological samples. These slides consist of aggregated exfoliated cells and tissue fragments from urine, other body fluids, cervical scrapes, and FNA specimens, which retain a cellular architecture such that it is similar to that in a surgical specimen. Therefore, CB can serve as an interface between cytology and histopathology that facilitates a definite diagnosis. Moreover, it can be used to perform ancillary studies, including special staining, immunohistochemical staining, and molecular tests.[20],[21] Collins et al.[22] also reported that, relative to the LBC-alone approach, the combination of LBC+CB for bronchial wash specimens improved the diagnosis of pulmonary malignancies by 100% with ancillary studies and by 67% without ancillary studies. Nathan et al.[23] studied 409 FNA specimens with CS and CB preparations, and reported sensitivities of 84.8% for CS alone and 73.3% for CB alone, with use of an adjunctive CB preparation increasing the overall sensitivity by 15.2%.

Few studies have evaluated the diagnostic utility and potential advantage of CB for thyroid FNA specimens. Sanchez and Selvaggi[24] analyzed 82 thyroid FNA specimens using CB preparations and reported that this approach contributed to the diagnosis in only 31% of all samples and in 22% of neoplastic cases. The authors attributed the lack of substantial contribution in the majority of cases to low cellularity. Horton et al.[25] evaluated 965 low-cellularity thyroid FNA specimens with paired ThinPrep and Cellient CB preparations, which were classified based on the initial ThinPrep examination as non-diagnostic (n = 398), benign (n = 294), and atypia/follicular lesion of undetermined significance (AUS/FLUS, n = 273). The CB preparation caused a diagnostic change in 15.3% of all cases (n = 148), with 31% of the initially non-diagnostic specimens (n = 123) being judged to be diagnostic (benign or AUS/FLUS) based on the CB preparation. However, the CB preparation only caused a diagnostic change in 8% of the initially AUS/FLUS specimens (n = 23) and 0.6% of the initially benign specimens. Similar conclusions were reached by Cristo et al.[26] and Jiang et al.,[27] who reported that combined use of CS and CB helped reduce the unsatisfactory rate of thyroid FNA specimens. Moreover, Jiang et al.[27] reported that, relative to CS alone, the combination of CS and CB had a higher malignancy rate during follow-up for cases with a cytological diagnosis of suspicious for malignancy (90.4% vs. 67.9%) and malignancy (99.5% vs. 97.7%). When the cytology laboratory initially switches from CS to LBC, it may be preferable to use a combination of LBC and CS to shorten the learning curve and enhance the diagnostic accuracy. If CS is not available in that institution, the findings from our study and previous studies indicate that adding CB in selected cases with thyroid FNA could probably help refine the diagnosis.

The main concern regarding this study is the use of a single ThinPrep slide for comparison with the CB slide. However, there are variable opinions regarding the required number of LBC slides to adequately assess cellularity and accurately diagnose thyroid FNA specimens. Hasteh et al.[28] evaluated 100 consecutive FNA specimens from various sites, including 40 thyroid samples, with two ThinPrep slides preparations per specimen, and found that 97% of the cases exhibited good reproducible results from the second slides. The authors therefore concluded that a single ThinPrep slide is appropriate and representative for making a definite diagnosis. However, Frost et al.[14] studied 135 thyroid FNA specimens with direct smears and four thin-layer slides, and reported that direct smears had better diagnostic accuracy than thin-layer slides (96% vs. 85%). An average of 1.4 thin-layer slides were adequate to make a definite diagnosis. Rossi et al.[29] also concluded that an additional LBC slide could reduce the non-diagnostic rate and resulted in an 18.5% increase in the overall diagnostic rate. Thus, further studies are needed to compare the contributions of CB to additional LBC slide regarding the diagnostic accuracy of thyroid FNA specimens. This study is also potentially limited by the relatively small proportion of specimens with papillary structures (37.1%) based on the ThinPrep method, which is lower than the 61.2% rate reported by Lee et al. based on the SurePath method.[30] We speculate that this may be partially related to methodological differences, as the SurePath slides are more likely to preserve a more complex three-dimensional papillary structure, while the ThinPrep slides are more difficult to evaluate based on the structure breaking down into smaller pieces.[1],[30] In addition, this study used a stricter definition of “papillary architecture” that excluded small papillary-like fragments without fibrovascular cores, which might have led to underestimation of the total number of specimens with papillary structures.

In conclusion, we found that an additional CB preparation from the residual LBC material was an effective method for increasing the diagnostic sensitivity for PTC. In addition to its complementary diagnostic role, the additional CB slide may also provide a “microbiopsy” perspective that provides a similar histological overview to that of the surgical specimen. Therefore, for cytopathologists who are less proficient in the morphology of LBC and when CS is unavailable, CB can be a valid adjunct method for better diagnosis of PTC.

Financial support and sponsorship

The authors received no financial support for the research, authorship, and/or publication of this article.

Conflicts of interest

The authors declare that there are no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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Correspondence Address:
Chi-Shun Yang
Department of Pathology and Laboratory Medicine, Taichung Veterans General Hospital, No. 1650 Taiwan Boulevard Sector 4, Taichung - 40705, Taiwan
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/IJPM.IJPM_999_19

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

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


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