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ORIGINAL ARTICLE Table of Contents   
Year : 2010  |  Volume : 53  |  Issue : 4  |  Page : 686-691
Papillary thyroid carcinoma: How much should the surgeon read from Fine needle aspiration cytology reports?


Departments of Pathology and Radiology and Center for Research, Faculty of Medicine, Kuwait University; Cytology Unit, Mubarak Al-Kabeer Hospital, Histopathology Units, Al-Jahra Hospital, Al-Amiri Hospital, Mubarak Al-Kabeer Hospital, and Hussain Makki Al-Juma Center for Specialized Surgery, Kuwait

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Date of Web Publication27-Oct-2010
 

   Abstract 

Objective: During routine fine needle aspiration cytodiagnosis of papillary thyroid carcinoma (PTC), a number of cases are diagnosed as suspicious; or it is suggested that PTC or a neoplasm be ruled out by histopathology. Since these diagnostic labels are likely to put the clinicians in a difficult situation while planning the management, this study aims to find out how much the surgeon should read from these reports. Materials and Methods: The patients were divided into two groups. Group A included 38 cases diagnosed as PTC or suspicious of PTC. Group B included 40 cases in which it was suggested that PTC/a neoplasm to be ruled out and non-neoplastic lesions with one or more cytologic features of PTC. The two groups were compared with clinical, imaging and cytomorphologic features. Results: A significant difference was observed with respect to age between Group A and Group B (P<0.001). The frequency of the following five cytologic features was significantly higher in Group A: papillary formation (P<0.001), psammoma bodies (P=0.054), fine nuclear chromatin (P=0.010), frequent nuclear grooves (P<0.001) and intra-nuclear cytoplasmic inclusion (P<0.001). Three or more of the five cytologic features were also reported in significantly higher number of Group A cases (P<0.001). Majority (81.8%) of the cases with subsequent histology in Group A were confirmed as PTC as opposed to 7.7% in Group B (P<0.001). Conclusions: Thus, cases with definitive cytodiagnosis of PTC and suggestive of PTC (Group A) should be taken much more seriously by the surgeons as compared to Group B cases.

Keywords: Fine needle aspiration cytology, papillary thyroid carcinoma, solitary thyroid nodules

How to cite this article:
Das DK, Sheikh M, Mallik MK, Sharma PN, Mannan AA, Sheikh ZA, Haji BI, George SS, Madda JP, Hussein S, Francis IM. Papillary thyroid carcinoma: How much should the surgeon read from Fine needle aspiration cytology reports?. Indian J Pathol Microbiol 2010;53:686-91

How to cite this URL:
Das DK, Sheikh M, Mallik MK, Sharma PN, Mannan AA, Sheikh ZA, Haji BI, George SS, Madda JP, Hussein S, Francis IM. Papillary thyroid carcinoma: How much should the surgeon read from Fine needle aspiration cytology reports?. Indian J Pathol Microbiol [serial online] 2010 [cited 2019 Jun 20];53:686-91. Available from: http://www.ijpmonline.org/text.asp?2010/53/4/686/72032



   Introduction Top


Fine needle aspiration (FNA) cytology is widely utilized as an important tool for the diagnosis of thyroid lesions, with a high degree of sensitivity, specificity, and diagnostic accuracy. [1],[2] Unlike follicular and Hόrthle cell carcinomas, papillary thyroid carcinoma (PTC) has well-defined FNA cytologic features, which are divided into five major and eight minor diagnostic criteria according to the synopsis of National Cancer Institute (NCI) Thyroid Fine-Needle Aspiration State of the Science Conference. [3],[4],[5],[6],[7],[8],[9],[10],[11],[12]

FNA cytology is considered the most valuable tool for the preoperative diagnosis of PTC. [13] However, during routine FNA cyto-diagnosis, a large number of cases are diagnosed as suspicious of (S/O) PTC or it is suggested that PTC be ruled out (R/O) by histopathology; there are also cases with one or more cytologic features of PTC, which are diagnosed as suspicious of a neoplastic lesion or benign lesions. Since these diagnostic labels are likely to put the clinicians in a difficult situation while planning the management strategy, this study was undertaken to find out if some diagnostic groups can be taken more seriously as compared to others and justify different approaches to be taken by the surgeon. In one recent report on PTC it was found that the PTC cases and, to some extent, S/O PTC cases were cytomorphologically distinct from other diagnostic labels. [14] In the present study, we compare the combined PTC and S/O PTC cases with rest of the diagnostic labels related to PTC based on clinical presentation, imaging findings, and cytologic features.


   Materials and Methods Top


Seven hundred and twenty nine cases were subjected to fine needle aspiration (FNA) of thyroid lesions during the year 2002 at the cytology clinic of our hospital. Of these, 21 were diagnosed as PTC, and 17 cases each as S/O PTC and R/O PTC. The other lesions with one or more cyto-morphologic features of PTC had the following diagnostic labels and frequency: R/O neoplasia (eight cases) and non-neoplastic lesions (15 cases). The age of these 78 cases ranged from 16 to 68 years with a median of 38 years and mean ± S.D of 39.5 ± 10.77 years. Male to female ratio was 11: 67. Imaging findings (ultrasonography and/or radionucleotide scan) were available in 53 cases prior to FNA. Histopathology report could be traced in 35 cases. Group-A patients included 38 cases diagnosed as PTC or S/O PTC and Group B patients included 40 cases diagnosed as R/O PTC, S/O or R/O neoplasm, and the non-neoplastic lesions with one or more cytologic features of PTC. The two groups were compared with age and sex distribution, as well as association with solitary thyroid nodules and their exact location in thyroid as revealed by imaging studies. As regards the cytologic features of PTC, those specified by NCI FNA State of Science Conference synopsis were followed. [12] From the five major diagnostic criteria, viz., (1) enlarged, oval "and irregular" nucleus, (2) eccentric and often multiple micronucleoli, (3) fine, pale chromatin, (4) longitudinal nuclear grooves, (5) intra-nuclear pseudo- or cytoplasmic inclusions (INCI), and eight minor diagnostic features, viz., (1) papillary cyto-architecture, (2) syncytial monolayers, (3) dense squamoid cytoplasm, (4) viscous or gummy ("bubble-gum") colloid, (5) psammoma bodies, (6) multinucleated giant cells, (7) histiocytoid cells and (8) cellular swirls, we took into consideration the frequencies of only five cytologic features of PTC as mentioned in the original FNA cytology reports. These included three major diagnostic criteria (nuclear grooves, fine nuclear chromatin and INCI) and two minor features (papillary formation, and psammoma bodies). In the presence of other cytologic features of PTC, micro-acinar formation was also taken into consideration as a substitute for papillary formation keeping in view the follicular variant of PTC. Two of the cyto-morphologic features, viz., fine nuclear chromatin and nuclear grooves, were semi-quantitatively assessed under the following three subdivisions: many/frequent throughout the smear, frequent in occasional group of cells, and occasional throughout the smear. Frequency of cases with three or more cytologic features was also compared between the two groups. Fisher's exact test of probability and Student's T-Test were employed for finding out the statistical significance.


   Results Top


Of the 38 cases in Group A, 22 had information on histopathology reports. Whereas 18 of these 22 cases [Figure 1] and [Figure 2] were diagnosed as PTC in histology, one was diagnosed as follicular adenoma, and three [Figure 3] as MNG. Of the 40 cases in Group B, 13 had subsequent histopathology reports available. Of these, one case [Figure 4] was diagnosed as PTC in histology and 12 [Figure 5] as MNG. Thus, 18 of the 22 cases (81.8%) with subsequent histology in Group A were confirmed as PTC as opposed to 1 of the 13 Cases (7.7%) in Group B (P< 0.001).
Figure 1 :Papillary thyroid carcinoma (PTC): The FNA smears showed four cytologic features which included papillary cytoarchitecture (a, MGG; ×200), INCI (b, MGG; ×400), frequent nuclear grooves and fine nuclear chromatin (c, Papanicolaou; ×400). The histopathological diagnosis was PTC

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Figure 2 :Suggestive or suspicious of (S/O) PTC: Frequent nuclear grooves and fine nuclear chromatin (a, Papanicolaou; ×400) were observed during initial reporting. Acinar formation and INCI (b, Papanicolaou; ×400) were noticed during review. The histopathological diagnosis was a follicular variant of PTC (PTC-FV).

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Figure 3 :S/O microscopic PTC in a colloid goiter. Smears showed papillary formation (a, MGG ×200) and a few nuclear grooves (b, Papanicolaou; ×200). Rare INCI was also described in original report. The histopathological diagnosis was multinodular goiter (MNG).

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Figure 4 :R/O PTC. Micro-acinar formation (a, MGG; ×200; b, Papanicolaou; ×400), fine nuclear chromatin (b), and nuclear grooves were observed during routine cyto-diagnosis. A single INCI was noticed during review (b inset, Papanicolaou; ×400). The histopathological diagnosis was PTC-FV

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Figure 5 :R/O microscopic PTC in colloid goiter. FNA smear showed frequent nuclear grooves and fine nuclear chromatin (Papanicolaou; ×400). The histopathological diagnosis was MNG

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[Table 1] depicts comparison of clinical and imaging findings between Group A and Group B. A significant difference was observed with respect to age (mean± standard deviation) between Group A (35.5 ± 8.91 years) and Group B (43.2 ± 11.12 years). The number of cases above the age of 45 years were significantly lower in Group A (10.8%) as compared to group B (40.0%). No significant difference was observed between the two groups in male: female ratio. There was also no significant difference in frequency of solitary nodules but a significantly higher number of solitary nodules were located in the left lobe in Group A (46.7%) than in Group B (19.2%). There was also a significant difference between the two groups with respect to association with non-neoplastic lesions.
Table 1 :Comparison of clinical features and imaging findings of cases diagnosed cytologically as Papillary Thyroid Carcinoma (PTC) and suggestive of (S/O) PTC with other thyroid lesions sharing cytologic features of PTC


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The frequencies of five cyto-morphologic features of PTC between Group A and Group B have been compared in [Table 2]. As compared to Group B, a significantly higher number of cases in Group A showed papillary formation (50% vs. 5.0%), psammoma bodies (15.8% vs. 2.5%), fine nuclear chromatin (55.3% vs. 25.0%), frequent nuclear grooves throughout the smear (65.8% vs. 22.5%) and intra-nuclear cytoplasmic inclusions (63.2% vs. 12.5%). ≥ 3 of the 5 cytologic features were reported in a significantly higher number of cases in Group A than Group B (65.8% versus 5.0%).
Table 2 :Comparison of cytomorphologic features of cases diagnosed cytologically as Papillary Thyroid Carcinoma (PTC) and suggestive of (S/O) PTC with other thyroid lesions sharing cytologic features of PTC


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   Discussion Top


In choosing the most appropriate management of a finding suspicious of PTC on FNA biopsy, the surgeon must be aware of the diagnostic importance of certain cyto-pathological features and the presence of a combination of features may allow a more confident surgical approach. [15] A look into all the FNA cytology reports of thyroid lesions during a period of one year, showed that in 38 cases the cyto-diagnosis was PTC or suspicious of PTC and in almost equal number (40 cases) it was suggested that PTC/thyroid neoplasm should be ruled out or a non-neoplastic lesion was considered in the presence of one or more cytologic features of PTC. On receiving these reports, if the surgeon realizes the relative importance of the terminologies used in the final cyto-diagnosis of the lesions and more so, the significance a specific or a combination of cytologic findings mentioned in the detailed report and the limitations of the cyto-pathologists with respect to these findings, it would be easier to plan the management of cases.

While comparing the two groups, we observed that there were certain differences between them in clinical and imaging findings and most of the cyto-morphological parameters. The mean age of PTC cases in our material (35.5 years) was about five years less than those in earlier reports; [16],[17] 40% of our Group B patients were above 45 years of age as compared to 10.8% in Group A (P=0.0043). The higher age in Group B patients may be attributed to the presence of large number of benign lesions, especially adenomatous goiter cases in that group. It has been observed that the cancer diagnosed within multi nodular goiter had higher age at diagnosis than solitary cancer nodule (48 versus 40 years, P= 0.002). [18] In our material, there was no significant difference in frequency of solitary nodules between the two groups (78.9% in Group A vs. 65.0% in Group B, P=0.2124) but a significantly higher number of solitary nodules were located in the left lobe in Group A (46.7%) than in Group B (19.2%, P= 0.0473). Predominance of left lobe involvement in our PTC and S/O PTC cases is in quite contrast to other studies on thyroid. [16],[19],[20]

The frequencies of four cytologic features in this study, viz., papillary formation, fine nuclear chromatin, frequent nuclear grooves throughout the smear, and intranuclear cytoplasmic inclusions were significantly higher in Group A than in Group B (P= 0.010 to < 0.001). Presence of psammoma body was also higher in Group A with a borderline significance (P= 0.054). Although this gives an impression that the diagnosis of PTC should be easy in presence of these cytologic features, all these five features may not be present in any PTC case [14] and one or two of these features can be missed during routine cytodiagnosis, as has been highlighted under legends for illustrations. Moreover, most of these features have certain limitations, which the clinician should be aware of. Multinodular goiter with multicentric papillary hyperplasia may present cytologic features suggestive of PTC. [21] Even in histology, encapsulated Hόrthle cell adenomas and follicular adenomas with papillary architecture may mimic papillary thyroid carcinoma but they have limited nuclear features of PTC. [22],[23] Psammoma body (PB) is almost diagnostic of PTC, but it is present in FNA smears of 11 to 35.0% of PTC cases only. [5] Clear nucleus (fine chromatin pattern in cytology) can be focally present in Graves' disease, chronic lymphocytic thyroiditis and some follicular adenomas [24] and "pseudoclear" nuclei may be noted in a variety of situations ranging from normal thyroid to diffuse hyperplasia (in 65% cases). [25] Grooved nuclei are present in 85-100% of PTC, 70 to 80% of non-papillary neoplasms and 50-60% of non-neoplastic thyroid lesions. [8] To overcome this difficulty, a dividing line of 20% nuclear grooves was proposed so as to diagnose maximum number of PTC cases.[26] Although intranuclear cytoplasmic inclusion is considered the most important cytologic feature of PTC (observed in 90% of cases), it may also be found in a variety of thyroid lesions such as medullary thyroid carcinoma, follicular adenoma, hyalinizing trabecular adenoma, and colloid goiter. [7] It is also known that FNA cytology has a very low sensitivity in follicular variant of PTC as compared to usual PTC and this limitation is almost of the same magnitude in frozen sections. [27] Two other major problems in cytodiagnosis of PTC include suboptimal material due to cystic change [2],[13] and microscopic/occult papillary carcinoma (OPC), with frequencies ranging between 5.6% and 35.6% in autopsy materials. [28] It may be very difficult to sample the small lesions of OPC without imaging guidance and even with US-guidance adequate neoplastic cells may not be aspirated resulting in false negative cytodiagnosis. [29] Thus, whenever there is no convincing cytologic evidence due to lack of adequate number of cytologic features of PTC, cytopathologists possibly like to remain on the safe side and resort to using diagnostic labels such as R/O PTC or R/O a neoplasm by histopathological examination and even diagnose it as a benign lesion.

If the surgeon appreciates the existence of these limitations, he would not make a big issue of the noncommittal cytology reports. Further, our findings, i.e., 18/22 (81.8%) had subsequent histologic confirmation of PTC in Group A as opposed to 1/13 (7.7%) cases in group B (P< 0.001), suggest that whenever diagnostic labels such as R/O PTC, R/O a neoplasm or a benign lesion in presence of one or more cytologic features of PTC is used, the chance of finding PTC in surgical specimen is remote.

In conclusion, Group A patients diagnosed as PTC and S/O PTC by FNA cytology were found to be distinct from cases with other diagnostic labels having one or more cytomorphologic features of PTC by being significantly younger, having significantly higher frequency of solitary nodules in the left lobe, higher frequency of cases with each of the five cytologic features under consideration, more number of cases with ≥ 3 out of 5 cytologic features of PTC, and significantly higher number of cases with histologic confirmation as PTC. Based on our findings, it is suggested that the clinicians should give due importance to Group A cases and manage Group B cases more conservatively unless there is strong clinical and/or imaging evidence of malignancy. The Group B cases should have a close follow-up and repeat FNA, preferably under imaging guidance.

 
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Correspondence Address:
Dilip K Das
Department of Pathology, Faculty of Medicine, Kuwait University, P.O. Box: 24923, Safat 13110
Kuwait
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0377-4929.72032

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