Indian Journal of Pathology and Microbiology
Home About us Instructions Submission Subscribe Advertise Contact e-Alerts Ahead Of Print Login 
Users Online: 1152
Print this page  Email this page Bookmark this page Small font sizeDefault font sizeIncrease font size


 
  Table of Contents    
ORIGINAL ARTICLE  
Year : 2019  |  Volume : 62  |  Issue : 2  |  Page : 211-215
Incidental papillary thyroid microcarcinomas in thyroidectomy specimens: A single-center experience from Turkey


1 Department of Pathology, Nose and Throat, Kayseri City Training and Research Hospital, Kayseri, Turkey
2 Department of Radiation Oncology, Nose and Throat, Kayseri City Training and Research Hospital, Kayseri, Turkey
3 Department of Nuclear Medicine, Nose and Throat, Kayseri City Training and Research Hospital, Kayseri, Turkey
4 Department of Ear, Nose and Throat, Kayseri City Training and Research Hospital, Kayseri, Turkey

Click here for correspondence address and email

Date of Web Publication10-Apr-2019
 

   Abstract 


Background: Papillary thyroid microcarcinoma (PTM) is a relatively common entity in the general population. PTM is often asymptomatic and is detected incidentally during the histopathological examination of thyroidectomy specimens from operations because of benign thyroid disease. Aims: The aims of the study are to determine the incidence of incidental papillary thyroid microcarcinomas (IPTMs) in our center, to examine the clinicopathologic characteristics of these tumors, and to present our experiences. Materials and Methods: This study includes 827 patients who underwent thyroidectomy operation in our center between January 2013 and June 2017 and were examined histopathologically in the Pathology Clinic. Patients' demographic characteristics, preoperative diagnoses, operative procedure, histopathological findings, and postoperative prognostic indexes are presented. Results and Conclusion: Of the 827 patients, 138 (16.6%) were diagnosed with a malignancy. Of these, 124 were papillary carcinoma, 5 were follicular carcinoma, 4 were lymphoma, 2 were medullary carcinoma, 2 were anaplastic carcinoma, and 1 was poorly differentiated carcinoma. The IPTM incidence rate was 8.01%; the multifocality and bilaterality rates were 23.3% and 13.3%, respectively. In 98.3% of IPTM cases, total thyroidectomies were performed, and in 1.7% of cases, subtotal thyroidectomy was performed followed by complementary thyroidectomy. No relapse or metastasis was detected in any of these cases. A careful histopathological examination of the thyroidectomy specimen is essential because IPTM is frequently skipped in fine needle aspiration cytology. We consider it best to perform total thyroidectomies because bilaterality and multifocality rates are high in IPTM. Long-term life expectancy in these tumors is quite good.

Keywords: Incidental papillary thyroid microcarcinoma, total thyroidectomy

How to cite this article:
Senel F, Karaman H, Aytekin A, Silov G, Bayram A. Incidental papillary thyroid microcarcinomas in thyroidectomy specimens: A single-center experience from Turkey. Indian J Pathol Microbiol 2019;62:211-5

How to cite this URL:
Senel F, Karaman H, Aytekin A, Silov G, Bayram A. Incidental papillary thyroid microcarcinomas in thyroidectomy specimens: A single-center experience from Turkey. Indian J Pathol Microbiol [serial online] 2019 [cited 2019 May 25];62:211-5. Available from: http://www.ijpmonline.org/text.asp?2019/62/2/211/255825





   Introduction Top


Thyroid carcinomas are the most common endocrine carcinoma and comprise 90% of all endocrine malignancies. The frequency of incidental thyroid carcinomas has been gradually increasing recently.[1],[2] In thyroid surgery, more frequent bilateral total excisions of the thyroid gland and detailed histopathological examinations of thyroid tissue are thought to be among the reasons for the recent increase.[3],[4] The prevalence of incidental papillary thyroid microcarcinomas (IPTMs) is reported to be 7.1%–16.3%.[5],[6]

If malignancy is not suspected clinically, tumors that are detected during the histopathological examination of specimens undergoing thyroidectomy operation are called “incidental.”[7] Papillary microcarcinoma is the most common type of incidental thyroid carcinoma.[8],[9] The tumor is called “papillary thyroid microcarcinoma” (PTM) if it is 1 cm or smaller.[10] The majority of PTMs are detected incidentally during histopathological examinations for benign thyroid disease.[4] The incidence of thyroid carcinoma in multinodular goiter (MNG) cases is reported to be 7.5%–13%.[11],[12] The diagnostic value of fine needle aspiration cytology (FNAC) decreases in the diagnosis of malignancy because of the increase in the number of nodules in MNG cases, and incidental thyroid carcinoma is a frequent finding in MNG.[11],[12] For this reason, many authors recommend total thyroidectomy for nonmalignant thyroid diseases such as MNG, chronic thyroiditis, and Graves' disease.[13]


   Materials and Methods Top


This study includes 827 patients who underwent thyroidectomies in our center between January 2013 and June 2017 and were examined histopathologically in the Pathology Clinic. Patients' information was obtained from computer records and phone calls when required. Age, sex, preoperative clinical diagnoses, FNAC diagnoses, operative procedure, and histopathological findings of these cases were recorded.

Cases diagnosed or with suspected malignancy were not included. Furthermore, cases with a tumor size greater than 1 cm in the histopathological examination were also excluded. Histopathological findings such as IPTM cases' preoperative diagnoses, age, sex, tumor type, tumor size, bilaterality, multifocality, thyroid capsule invasion, and lymphovascular invasion were evaluated.

Postoperative prognostic indices were investigated, such as relapse, metastasis, and survival. The follow-up period is from the date of diagnosis to the date of relapse or the last follow-up. The patients were followed up for a mean period of 34 months (range 9–59 months). Free thyroxin (FT4) and serum thyroid-stimulating hormone (TSH) levels were analyzed to determine the suppressive dose of LT4 in the first and third postoperative months (suppression of TSH at <0.25 mIU/mL). Serum TSH, FT4, thyroglobulin (Tg), and anti-thyroglobulin antibody (anti-TgAb) were analyzed in the postoperative sixth month. Cervical lymph nodes were examined by ultrasonography (USG). Cervical USG was performed annually, and serum levels of TSH, FT4, TG, and TgAb were examined.


   Result Top


For about 4.5 years, 827 thyroidectomies were performed in our center and 138 (16.6%) patients were diagnosed with a malignancy. Of these patients, 5 (3.6%) were diagnosed with follicular carcinoma, 4 (2.9%) were diagnosed with lymphoma, 2 (1.5%) were diagnosed with anaplastic carcinoma, 2 (1.5%) were diagnosed with medullary carcinoma, 1 (0.7%) was diagnosed with poorly differentiated carcinoma, and 124 (89.8%) were diagnosed with papillary carcinoma. Of the papillary carcinoma cases, 55 (44.3%) were diagnosed with classical papillary carcinoma (tumor size greater than 1 cm) and 69 (55.6%) were diagnosed with papillary microcarcinoma (tumor size 1 cm or smaller) [Table 1]. FNAC was not performed in 13 of the 69 papillary microcarcinoma cases. Nine cases were diagnosed with malignancy by FNAC and this group was not included in the study. In all, 47 papillary microcarcinoma cases were reported as benign by FNAC. In this study, the IPTM rate was 8.01% (60 cases).
Table 1: Malign tumors detected in thyroidectomy specimens

Click here to view


The average age in cases with IPTM was 48 years (range 26–69 years). Of these, 53 (88.3%) were female and 7 (11.7%) were male. Of the 60 IPTM cases, 57 (95%) were operated with a prediagnosis of nontoxic MNG, whereas 3 (5%) were operated with a prediagnosis of toxic MNG. Total thyroidectomies were performed in 59 cases (98.3%). One case (1.7%) underwent a subtotal thyroidectomy and then a complementary thyroidectomy; a papillary microcarcinoma focus was observed in the other lobe of this case. In cases with incidental thyroid papillary microcarcinoma, the tumor size range was 1–10 mm with an average of 4.6 mm. The tumor was in the left lobe in 32 cases (53.3%), in the right lobe in 20 cases (33.3%), multifocal in 14 cases (23.3%), and bilateral in 8 cases (13.3%). Thyroid capsule invasion was detected in five cases (8.3%). Tumors were multifocal in four cases with capsule invasion.

Generally, cells with nuclear clearing were arranged around the fibrovascular core in histopathological examinations [Figure 1]. Tumor cells were positively stained with immunohistochemical markers such as cytokeratin 19 [Figure 2]. No lymphovascular invasion was detected in any of the cases. Other histopathological findings accompanying IPTM cases were MNG in 41 cases (68.3%), lymphocytic thyroiditis in 16 cases (26.6%), and follicular adenoma in 3 cases (5%) [Table 2].
Figure 1: Cells with nuclear clearing generally arranged around the fibrovascular core observed in histopathological examination (H and E, ×400)

Click here to view
Figure 2: Positive staining with cytokeratin 19 immunohistochemical markers in tumor cells (IHC, ×400)

Click here to view
Table 2: Clinicopathologic characteristics of incidental papillary thyroid microcarcinoma cases

Click here to view


All patients were given I-thyroxin (LT4) to suppress the TSH. Five patients with thyroid capsule invasion were treated with radioactive iodine (RAI) for 4–6 weeks after the operation. During follow-up, cervical USG was performed every 6 months for the first 2 years and then annually; serum levels of TSH, FT4, TG, and TgAb were also examined. No relapse or metastasis was detected in any of these cases, and all the patients are alive.


   Discussion Top


Papillary thyroid carcinoma is the most frequent histopathologic type of malignant thyroid carcinoma.[9],[10] The small version is called papillary thyroid microcarcinoma which is 1 cm or smaller.[9]

The ratio of IPTM is reported to be 7.1%–16.3% in the literature.[5],[6] The IPTM ratio in this study was 8.01%, which is consistent with the literature. In the literature, the ratio of incidental carcinomas among all papillary thyroid carcinomas is reported to be 49%–75.5%.[14],[15],[16] In this study, the ratio of incidental carcinomas among all papillary thyroid carcinomas was 48.4%. It is reported that the ratio of IPTM cases has increased in recent years and the increase in total thyroidectomies is a contributing factor.[3]

Papillary thyroid microcarcinoma is often asymptomatic and is detected incidentally during the histopathological examination of thyroidectomy specimens from operations because of benign thyroid disease.[4],[17] In our study, only benign thyroid lesions were detected in 689 (83.3%) of all cases (827) who underwent thyroidectomy operation. Benign lesions according to IPTM cases were MNG in 41 cases, lymphocytic thyroiditis in 16 cases, and follicular adenoma in 3 cases.

In this study, 69 papillary microcarcinoma cases were detected and 9 (16%) were diagnosed with papillary microcarcinoma by preoperative FNAC. The remaining 60 cases were detected incidentally during the histopathological examination of the thyroidectomy specimen. In our study, 83.9% of papillary microcarcinoma cases were skipped in FNAC. As confirmed by this study, the diagnostic value of FNAC for papillary microcarcinoma is low. Because most patients have MNG and tumors are small, it is difficult to sample the area with FNAC.[9],[12] Similar to the study by Senel F et al., papillary microcarcinomas associated with thyroiditis are generally not detectable by FNAC.[18]

Careful histopathological examinations are essential for the diagnosis of papillary thyroid microcarcinoma. Because of the possibility of IPTM, careful macroscopic examinations should be performed with multiple sections on thyroidectomy specimens. Sometimes the tumor is macroscopically recognized as a broken white-colored area of just a few millimeters and sometimes it is only detectable with a microscopic examination.

The important properties of papillary thyroid microcarcinomas are multifocality and bilaterality. Multifocality is the presence of tumor in more than one focus in the same thyroid lobe or the presence of tumor in both lobes. In the literature, the multifocality rate in IPTM is reported to be 13%–41%.[16],[19],[20] In this study, the multifocality rate was 23.3% and the risk of cancer in the opposite lobe was 50% in patients with more than one focus in the same lobe. The determination of multifocality in papillary microcarcinoma is difficult in the preoperative period. Bilaterality is the presence of tumor in both the lobes. In the literature, the bilaterality rate is reported to be 20%–27.5%.[19],[20] In this study, the rate of bilaterality is lower than that reported in the literature and this rate is 13.3%. The reason for this variability is thought to be because of the use of different diagnostic criteria in different studies and may be because of the possibility of missing sight.

Lymph node involvement is common in papillary carcinoma cases. The regional lymph node metastasis was observed in 29%–40. 9% of cases.[21],[22] The lower incidence of nodal metastasis was seen in papillary thyroid microcarcinoma.[5] This rate was reported to be 0% in the study by Wang et al. and 10. 7% in the study by Vlassopoulou et al.[23],[24] Similar to the study by Wang et al.[23] no lymph node involvement was detected in any of our IPTM cases.

Total thyroidectomies are preferred in our center because of high bilaterality and multifocality rates in papillary thyroid microcarcinoma. In the literature, the mean tumor size in IPTM is below 5 mm.[16],[23] Consistent with this, the mean tumor size in this study was 4.6 mm.

Treating patients with differentiated thyroid carcinoma involves primary adjuvant procedures such as hemithyroidectomy, complementary thyroidectomy, RAI therapy, LT4 therapy, and suppressing TSH levels. However, a very low rate of recurrence in a large series of IPTM cases does not suggest the use of adjuvant treatment, except the suppression of TSH levels with LT4 treatment.[25]

Central neck dissection or modified neck dissection is recommended if there is cervical lymphadenopathy.[26],[27] Neck dissection was not performed because no cervical lymphadenopathy was detected in our cases. Total thyroidectomies were performed in 98.3% of cases; subtotal thyroidectomy was performed in 1.7% of cases (one case). In this case, complementary thyroidectomy was performed, and papillary microcarcinoma focus was detected in the lobe.

Adjuvant radioiodine therapy is recommended if there is tumor multifocality, lymph node metastasis, and vascular invasion.[28] RAI is unnecessary in the majority of patients because of low risk of recurrence.[25] In this study, five patients with thyroid capsule invasion were treated with RAI.

The recurrence rate in IPTM is very low and is reported to be 0%–5%.[5],[15],[16] In this study, no recurrence or metastasis was observed in any of the cases.

In conclusion, the incidence rate of IPTM is high because of benign thyroid disease. FNAC is not very reliable in diagnosing papillary thyroid microcarcinoma. Therefore, a careful histopathological examination is essential. Multifocality and bilaterality are the main pathological features of papillary thyroid microcarcinoma, and total thyroidectomies are preferred.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Askitis D, Efremidou E.I, Karanikas M, Mitrakas A, Tripsianis G, Polychronidis A. Incidental thyroid carcinoma diagnosed after total thyroidectomy for benign thyroid diseases: Incidence and association with thyroid disease type and laboratory markers. Int J Endocrinol 2013;2013:451959.  Back to cited text no. 1
    
2.
Sipos.J.A, Mazzaferri. Thyroid cancer epidemiology and prognostic variables. Clin Oncol 2010;22:395-404.  Back to cited text no. 2
    
3.
Neuhold N, Schultheis A, Hermann M, Krotla G, Koperek O, Birner P. Incidental papillary microcarcinoma of the thyroid – Further evidence of a very low malignant potential: A retrospective clinicopathological study with up to 30 years of follow-up. Ann Surg Oncol 2011;18:3430-36.  Back to cited text no. 3
    
4.
Londero SC, Krogdahl A, Bastholt L, Overgaard J, Trolle W, Pedersen HB. Papillary thyroid microcarcinoma in Denmark 1996–2008: A national study of epidemiology and clinical significance. Thyroid 2013;23:1159-64.  Back to cited text no. 4
    
5.
Vasileiadis I, Karatzas T, Vasileiadis D, Kapetanakis S, Charitoudis G, Karakostas E, et al. Clinical and pathological characteristics of incidental and nonincidental papillary thyroid microcarcinoma in 339 patients. Head Neck 2014;36:564-70.  Back to cited text no. 5
    
6.
Slijepcevic N, Zivaljevic V, Marinkovic J, Sipetic S, Diklic A and Paunovic I. Retrospective evaluation of the incidental finding of 403 papillary thyroid microcarcinomas in 2466 patients undergoing thyroid surgery for presumed benign thyroid disease. BMC Cancer 2015;15:330.  Back to cited text no. 6
    
7.
Mantinan B, Rego-Ireata A, Larranaga A, Fluiters E, Sanchez-Sobrino P, Garcia-Mayor RV. Factors influencing the outcome of patients with incidental papillary thyroid microcarcinoma. J Thyroid Res 2012;2012:1-5.  Back to cited text no. 7
    
8.
Nanjappa N, Kumar A, Swain SK, Aroul TT, Smile SR, Kotasthane D. Incidental thyroid carcinoma. Indian J Otolaryngol Head Neck Surg 2013;61:37-9.  Back to cited text no. 8
    
9.
Gelmini R, Franzoni C, Pavesi E, Cabry F, Saviano M. Incidental thyroid carcinoma: A retrospective study in a series of 737 patients treated for benign disease. Ann Ital Chir 2010;81:42127.  Back to cited text no. 9
    
10.
Ito Y, Takuya H, Yuuki T, Akihiro M, Kaoru K, Fumio M. Prognosis of patient with benign thyroid disease accompanied by incidental papillary carcinoma undetectable on preoperative imaging tests. World J Surg 2007;31:1672-6.  Back to cited text no. 10
    
11.
Yousuf S, Hassan A. Total and near-total thyroidectomy is better than subtotal thyroidectomy for the treatment of bilateral benign multinodular goiter. Br J Med Med Res 2011;1:1-6.  Back to cited text no. 11
    
12.
Tezelman S, Borucu I, Senyurek Giles Y, Tunca F, Terzioglu T. The change in surgical practice from subtotal to near-total or total thyroidectomy in the treatment of patients with benign multinodular goiter. World J Surg 2009;33:400-5.  Back to cited text no. 12
    
13.
Abdelshaheed F. Total thyroidectomy for clinically benign thyroid disease: A preferred option with capsular dissection technique. Egypt J Surg 2006;25:149-53.  Back to cited text no. 13
    
14.
Dunki-Jacobs E, Grannan K, McDonough S, Engel AM. Clinically unsuspected papillary microcarcinomas of the thyroid: A common finding with favorable biology? Am J Surg 2012;203:140-4.  Back to cited text no. 14
    
15.
Lombardi CP, Bellantone R, De Crea C, Paladino NC, Fadda G, Salvatori M, et al. Papillary thyroid microcarcinoma: Extrathyroidal extension, lymph node metastases, and risk factors for recurrence in a high prevalence of goiter area. World J Surg 2010;34:1214-21.  Back to cited text no. 15
    
16.
John AM, Jacob PM, Oommen R, Nair S, Nair A, Rajaratnam S. Our experience with papillary thyroid microcancer. Indian J Endocrinol Metab 2014;18:410-3.  Back to cited text no. 16
    
17.
Malandrino P, Pellegriti G, Attard M, Violi MA, Giordano C, Sciacca L. Papillarythyroid microcarcinomas: A comparative study of the characteristics and risk factors at presentation in two cancer registries. J Clin Endocrinol Metab 2013;98:1427-34.  Back to cited text no. 17
    
18.
Senel F, Karaman H, Ertan T. Co-occurrence of subacute granulomatous thyroiditis and papillary microcarcinoma. Journal of Ear, Nose, and Throat 2016;26:248-50.  Back to cited text no. 18
    
19.
Costamagna D, Pagano L, Caputo M, Leutner M, Mercalli F, Alonzo A. Incidental cancer in patients surgically treated for benign thyroid disease: Our experience at a single institution. G Chir 2013;34:21-6.  Back to cited text no. 19
    
20.
Sakorafas G, Stafyla V, Kolettis T, Tolumis G, Kassaras G, Peros G. Microscopic papillary thyroid cancer as an incidental finding in patients treated surgically for presumably benign thyroid disease. J Postgrad Med 2007;53:23-6.  Back to cited text no. 20
[PUBMED]  [Full text]  
21.
El-Foll HA, El-Sebaey HI, El-Kased AF, Hendawy A, Kamel MM. Pattern and distribution of lymph node metastases in papillary thyroid cancer. J Clin Exp Pathol 2015;5:204.  Back to cited text no. 21
    
22.
Jagtap SV, Patil D, Chetan, Gupta SO. Papillary carcinoma thyroid presented with extensive local lymph nodal metastasis. IP Arch Cytol Histopathol Res 2018;3:113-5.  Back to cited text no. 22
    
23.
Wang S-F, Zhao W-H, Wang W-B, Teng X-D, Teng L-S, Ma Z-M. Clinical features and prognosis of patients with benign thyroid disease accompanied by an incidental papillary carcinoma. Asian Pac J Cancer Prevent 2013;14:707-11.  Back to cited text no. 23
    
24.
Vlassopoulou V, Vryonidou A, Paschou SA, Ioannidis D, Koletti A, Klonaris N, et al. No considerable changes in papillary thyroid microcarcinoma characteristics over a 30-year time period. BMC Res Notes 2016;9:252.  Back to cited text no. 24
    
25.
Di Donna V, Santoro MG, de Waure C, Ricciato MP, Paragliola RM, Pontecorvi A. A new strategy to estimate levothyroxine requirement after total thyroidectomy for benign thyroid disease. Thyroid 2014;24:1759-64.  Back to cited text no. 25
    
26.
Shaha AR. Management of the neck in thyroid cancer. Otolaryngol Clin North Am 1998;31:823-31.  Back to cited text no. 26
    
27.
Ito Y, Tomoda C, Uruno T, Takamura Y, Miya A, Kobayashi K. Papillary microcarcinoma of the thyroid: How should it be treated? World J Surg 2004;28:1115-21.  Back to cited text no. 27
    
28.
Hay ID, Grant CS, van Heerden JA, Goellner JR, Ebersold JR, Bergstralh EJ. Papillary thyroid microcarcinoma: A study of 535 cases observed in a 50-year period. Surgery 1992;112:1139-47.  Back to cited text no. 28
    

Top
Correspondence Address:
Fatma Senel
Department of Pathology, Kayseri City Training and Research Hospital, Kayseri
Turkey
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/IJPM.IJPM_439_18

Rights and Permissions


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2]



 

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...
   Result
   Discussion
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed331    
    Printed6    
    Emailed0    
    PDF Downloaded78    
    Comments [Add]    

Recommend this journal