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original report memo (2020) 13:126–133 https://doi.org/10.1007/s12254-019-00567-y Incidental thyroid papillary microcarcinoma on 1777 surgically treated patients for benign thyroid disease A monoinstitutional experience and literature review Gaia Peluso · Stefania Masone · Silvia Campanile · Carmen Criscitiello · Concetta Dodaro · Armando Calogero · Paola Incollingo · Gianluca Minieri · Marsela Menkulazi · Alessandro Scotti · Vincenzo Tammaro · Ali Akbar Jamshidi · Luigi Pelosio · Marcello Caggiano · Nicola Carlomagno · Michele L. Santangelo Received: 16 August 2019 / Accepted: 19 December 2019 / Published online: 31 January 2020 © The Author(s) 2020 Summary Results Total thyroidectomy was performed in 1649 Background We evaluated the frequency of inciden- patients (92.7%) and hemithyroidectomy in 128 (7.2%). tal papillary thyroid microcarcinomas (mPTC) in thy- Papillary thyroid cancer, sized between 2–10 mm, was roidectomies performed for benign diseases, to better found in 89 patients (5%), which were all by defini- characterize this nosologic entity and to assess the tion microcarcinomas (mPTC). In 11 patients mPTCs best treatment. were multifocal and in 7 bilateral. Just 6 patients Methods Between 2009 and 2017, a total of 1777 pa- received hemithyroidectomy and later underwent tients underwent surgery for benign thyroid disease. radical surgery without complications. No tumor-re- Patients with preoperative undetermined or positive lated morbidity or mortality was observed. The χ test for malignancy cytology were excluded, as well as in- showed a statistically significant association between cidental thyroid cancer larger than 1 cm. mPTC and non-toxic multinodular goiter. G. Peluso () · S. Campanile · C. Dodaro · A. Calogero · V. Tammaro P. Incollingo · G. Minieri · M. Menkulazi · A. Scotti · vincenzo.tammaro@unina.it V. Tammaro · A. Jamshidi · L. Pelosio · M. Caggiano · N. Carlomagno · M. L. Santangelo A. Jamshidi Advanced Biomedical Science Department, University akbar.jamshidi@live.it Federico II of Naples, Via S. Pansini 5, 80131 Naples, Italy L. Pelosio gaia.peluso5@gmail.com gigipelosio@hotmail.com S. Campanile M. Caggiano silvia.camp3@gmail.com marcello.caggiano@live.it C. Dodaro N. Carlomagno cododaro@unina.it nicola.carlomagno@unina.it A. Calogero M. L. Santangelo armando.calogero2@unina.it michele.santangelo@unina.it P. Incollingo S. Masone p.incollingo@studenti.unina.it Clinical and Surgical Medicine Department, University Federico II of Naples, Via S. Pansini 5, 80131 Naples, Italy G. Minieri stefaniamasone@yahoo.it minieri.gianluca87@gmail.com C. Criscitiello M. Menkulazi Division of Early Drug Development for Innovative mars.menk@gmail.com Therapies, European Institute of Oncology, 20141 Milan, Italy A. Scotti carmen.criscitiello@ieo.it alexscotti@inwind.it 126 Incidental thyroid papillary microcarcinoma on 1777 surgically treated patients for benign thyroid disease K original report Discussion In the literature, the rates of incidental tients were surgically treated for thyroid diseases. Of mPTC vary, due to various factors such as histopatho- these, we excluded 631 patients, who presented nod- logical examination and sampling numbers. Regard- ules bigger than 1 cm or had undetermined or positive ing surgical treatment, some authors support a “con- malignancy preoperative cytology (Thy 3–5 accord- servative” approach for the positive prognosis, but ing to the British Thyroid Association Thyroid FNAC considering that it can be associated with mortality, Reporting Guidelines) [9]. In all, 1777 patients (1374 lymph node recurrence and metastasis, its treatment women [77.3%] and 403 men [22.7%]) underwent is still controversial. thyroidectomy for benign diseases: a total thyroidec- Conclusions Our experience confirms that total thy- tomy was performed in 1649 subjects (92.7%) and a roidectomy in multinodular goiter is a safe procedure, hemithyroidectomy in 128 (7.2%). The indications for which ensures endocrine control and oncologic com- surgery were multinodular non-toxic goiter in 1469 plete tumor resection, in case of mPTC. In uninodular patients (82.66%), multinodular toxic goiter in 177 goiter, we recommend hemithyroidectomy; if mPTC (9.96%), uninodular non-toxic goiter in 104 (5.85%), is discovered, we suggest radical surgery especially in and uninodular toxic goiter (Plummer’s disease) in patients older than 50 years and with familial dispo- 27 patients (1.51%). sition for thyroid cancer and peripheral tumors larger Thyroid nodules, studied by ultrasound, showed no than 5 mm and aggressive variants. suspicious sign of malignancy. In the multinodular toxic or non-toxic goiter a total Keywords Thyroid · Incidental carcinoma · thyroidectomy was performed, whereas in uninodular Microcarcinoma · Total thyroidectomy · toxic and non-toxic goiter a hemithyroidectomy was Hemithyroidectomy the treatment of choice. Histopathological examination included the follow- Abbreviations ing: sections of fresh samples about 1 cm thick, which ITC incidental thyroid cancer were fixed in formalin 4% for 24 h, embedded in paraf- mPTC papillary thyroid microcarcinoma fin and then further sectioned up to 4–5 µm. PTC papillary thyroid carcinoma 2 The χ test was used to evaluate the association be- tween the incidence of mPTC in total thyroidectomy and hemithyroidectomy and in toxic and non-toxic Introduction goiter. Incidental thyroid cancer (ITC) is a malignant tumor The study has been performed in accordance with occasionally discovered through pathological exami- the Declaration of Helsinki and “good clinical prac- nation after thyroidectomy for benign thyroid disease tice” guidelines. All patients signed a consent form [1]. Usually they are papillary thyroid microcarcino- for the surgical procedure and for the storage and sci- mas (mPTC), which were defined in 1988 by the World entific use of their data. Health Organization as a papillary tumor with a diam- eter up to 10 mm (“minute” <5 mm and “tiny” between Results 5 and 10 mm), low aggressiveness and very low risk of distant metastases [2]. A review of the available data Histopathological examination identified 89 patients in the literature report the incidence of ITC to be be- of ITC (5%; 89/1777); all were papillary thyroid car- tween 7 and 21.6% in surgical specimens [1, 3, 4]. cinomas (PTCs), with a diameter less than or equal Despite the excellent prognosis, cases of mPTC with to 10 mm, therefore considered microPTC (mPTC). lymph node metastases are described: this occurred This group included 18 males (20.2%) and 71 fe- in adult patients with apparently benign cervical cysts males (79.8%). The median age was 46.7 years old and no palpable disease in the thyroid gland; more- (range 19–75 years old, standard deviation [SD] 13.53). over, recurrences in the residual parenchyma or dis- In all, 28 patients (31.4%) were 40 years old or younger. tant metastasis are reported [1, 5–8]. For this reason, All preoperative cytologies, if performed, were nega- the detection and clinical management of occult thy- tive for malignant cells. Surgical procedures were total roid carcinomas remain a controversial topic. In the thyroidectomy in 83 patients (93.2%) and hemithy- present study, we retrospectively review the data of roidectomy in 6 (6.8%). Preoperative diagnosis was patients who underwent surgery for benign thyroid multinodular non-toxic goiter in the 83 cases of to- diseases in our university hospital with the aim to es- tal thyroidectomy; in the 6 hemithyroidectomies the timate the frequency of incidental thyroid cancer, to diagnosis was uninodular non-toxic goiter. characterize the lesions, and to discuss the most suit- The percentage of mPTC in total thyroidectomy able approach. was 5.03% (83/1649), while in patients undergoing to- tal thyroidectomy for multinodular non-toxic goiter it was 5.6% (83/1469). In partial thyroidectomy, the per- Patients and methods centage of mPTC was 4.6% (6/128) while it was 5.7% Between January 2009 and December 2017, at the in patients undergoing hemithyroidectomy for unin- University Hospital of Naples Federico II, 2487 pa- odular non-toxic goiter (6/104). Thus, the incidence K Incidental thyroid papillary microcarcinoma on 1777 surgically treated patients for benign thyroid disease 127 original report Table 1 Clinical details of patients with microcarcinomas (mPTC) Patient no. Sex Age Surgical procedure Diameter (mm) Multifocal Bilateral Associated pathologic pictures 1 M 41 HT 1 YES NO – 2 F 45 TT 5 NO NO LT 3 F 55 TT 4 NO NO LT 4 F 29 TT 3 YES NO – 5 F 60 TT 4 NO NO RNP 6 F 59 TT 3 NO NO – 7 M 55 TT 2 NO NO – 8 F 24 TT 9 NO NO LT 9 M 30 TT 7 NO NO – 10 F 50 HT 3 NO NO – 11 F 41 TT 3 NO NO – 12 F 30 TT 2 NO NO – 13 F 48 TT 9 NO NO – 14 F 48 TT 7 NO NO – 15 F 52 TT 2 NO NO – 16 F 19 TT 9 NO NO – 17 F 33 TT 8 YES YES – 18 F 48 TT 7 NO NO HCA 19 F 51 TT 3 NO NO – 20 F 48 TT 8 NO NO RNP 21 F 28 TT 4 NO NO RNP 22 F 53 TT 6 NO NO RNP 23 F 34 TT 5 NO NO – 24 F 65 TT 3 NO NO – 25 M 61 TT 6 NO NO – 26 F 38 TT 4 NO NO – 27 F 37 TT 5 NO NO – 28 M 68 TT 3 YES NO – 29 F 59 TT 3 NO NO LT 30 F 58 TT 6 NO NO – 31 F 32 TT 4 NO NO – 32 F 48 TT 5 NO NO – 33 F 56 TT 8 YES YES LT 34 F 66 TT 2 NO NO HCA/RNP 35 F 25 HT 2 NO NO – 36 M 52 TT 7 NO NO RNP 37 F 34 TT 2 YES NO – 38 F 40 TT 2 NO NO RNP 39 M 59 TT 3 NO NO LT/RNP 40 M 69 TT 2 NO NO – 41 F 52 TT 4 NO NO LT 42 F 43 TT 2 NO NO LT 43 F 30 TT 4 NO NO – 44 F 28 TT 3 NO NO RNP 45 M 68 TT 9 NO NO – 46 F 47 TT 6 NO NO – 47 F 56 TT 4 NO NO RNP 48 F 26 HT 7 NO NO – 49 M 47 TT 5 NO NO LT/RNP 50 F 35 TT 1 NO NO LT 51 F 46 TT 7 NO NO – 128 Incidental thyroid papillary microcarcinoma on 1777 surgically treated patients for benign thyroid disease K original report Table 1 (Continued) Patient no. Sex Age Surgical procedure Diameter (mm) Multifocal Bilateral Associated pathologic pictures 52 F 43 TT 2 NO NO – 53 M 63 TT 3 NO NO RNP 54 F 57 TT 5 NO NO RNP 55 F 46 TT 5 NO NO LT 56 F 42 TT 10 NO NO RNP 57 F 29 TT 4 NO NO – 58 F 48 TT 4 NO NO – 59 F 75 TT 2 NO NO LT 60 M 50 TT 8 NO NO RNP 61 M 41 TT 1 NO NO LT 62 F 54 TT 4 NO NO RNP 63 F 61 TT 2 YES YES LT 64 F 29 TT 6 NO NO LT 65 F 49 TT 10 NO NO LT 66 F 64 TT 2 NO NO – 67 M 67 HT 3 NO NO LT 68 F 34 TT 3 NO NO – 69 F 66 TT 7 YES YES – 70 F 38 TT 6 NO NO – 71 M 56 TT 4 NO NO – 72 F 37 TT 3 YES YES – 73 F 37 TT 8 NO NO LT 74 F 48 TT 3 NO NO LT/RNP 75 F 34 TT 7 NO NO LT 76 F 57 TT 3 NO NO – 77 M 48 TT 8 NO NO LT 78 F 48 TT 6 YES YES – 79 F 73 TT 6 NO NO LT 80 F 66 TT 2 NO NO HCA/RNP 81 F 25 HT 2 NO NO – 82 M 52 TT 7 NO NO RNP 83 F 34 TT 2 YES NO – 84 F 40 TT 2 NO NO RNP 85 M 59 TT 3 NO NO LT/RNP 86 M 69 TT 2 NO NO – 87 F 19 TT 9 NO NO – 88 F 33 TT 8 YES YES – 89 F 48 TT 7 NO NO HCA TT total thyroidectomy, HT hemithyroidectomy, LT lymphocytic thyroiditis, HCA Hurthle cell adenoma, RNP regressive nonspecific phenomena of mPTC in patients with non-toxic thyroid disease and regressive, nonspecific phenomena in 19 (21.4%) was 5.6% (89/1573). No ITCs have been observed in (Tables 1 and 2). multinodular and uninodular toxic goiter. The mostfrequentvariant of mPTC was the clas- The mPTCs had a diameter between 2 and 10 mm, sical form, which was found in 61 patients (68.5%), all cases meeting the Porto Proposal criteria [10]. followed by the follicular variant in 25 patients (28%) There were no capsular or vascular invasion or lymph and diffuse sclerosing, mixed and oncocitic Warthin- node metastasis. In 11 patients (12.3%) multifocal like variant each found in1 case (1.1%) (Fig. 1). mPTCs were present, 7 (7.8%) of which were bilateral. The 6 patients who received a hemithyroidec- Other pathological pictures associated with goiter/ tomy, underwent a completion thyroidectomy, with- mPTC were the following: Hurthle cell adenoma in out complication and without sign of tumor at the 2 patients (2.2%), lymphocytic thyroiditis in 21 (23.5%) histopathological examination. K Incidental thyroid papillary microcarcinoma on 1777 surgically treated patients for benign thyroid disease 129 original report Table 2 Characteristics of microcarcinomas (mPTC) vs Table 3 Review of the literature type of surgery Authors and year Number of Incidence of Total Thyroidec- Hemithyroidectomy Total patients mPTC (in %) tomy Miccoli et al. 2006 [1] 998 10.4 Age 46.8 years 47.04 years 46.7 years Cerci et al. 2007 [11] 170 10.58 (SD 13.59 years) (SD 17.14 years) (SD 13.53 years) Sakorafas et al. 2007 [6] 380 7.1 Sex F 79.5% F 66.6% F 79.8% Bradly et al. 2009 [12] 678 12.0 M 20.4% M 33.3% M 20.2% Tezelman et al. 2009 [13] 2592 7.2 Diameter 4.67 mm 4.7 mm 4.62 mm mPTC (SD 2.41 mm) (SD 2.38 mm) (SD 2.42 mm) Pezzolla et al. 2010 [14] 165 18.2 Multifocality 13.2% 16% 12.3% Gelmini et al. 2010 [3] 737 11.1 SD standard deviation, F female, M male Askitis et al. 2013 [15] 228 14.5 Antonelli 2016 [4] 199 14.07 There was no difference between the incidence of Maturo et al. 2017 [16] 1793 4.63 mPTC in total thyroidectomy and hemithyroidectomy Peluso et al. 2019 1777 5 (P=0.7, χ test) or the incidence in women and men mPTC microcarcinoma (P=0.5). We also performed a χ test to compare the inci- dence of mPTC in non-toxic and toxic goiter and the excluded TIR3 patients. An accurate diagnostic pro- association was statistically significant (P = 0.0009). cedure allowed us to preoperatively diagnose a large Follow-up comprised clinical examination, blood number of mPTCs that were therefore excluded from and instrumental tests for a minimum of 1.5 years and our study. a maximum of 10 years and we have not observed any Considering only our patients with non-toxic thy- morbidity or mortality linked to the mPTCs. roid disease, the incidence of mPTC is 5.6% and this is closer to the values found in the literature: Tezel- man et al. have found a frequency of 7.2%, [13], while Discussion Bradly et al. reported an incidence of 10% in multin- In our experience, in the 5% (n = 89) of the patients odual goiter [12]. who underwent surgery for benign thyroid disease the A crucial point, in our opinion, is the preparation of final histology revealed a mPTC. In our data, the val- surgical specimens analyzed by the pathologist. This ues were slightly lower than the average reported in may partially explain the disparity of published data. theliterature(Table 3;[1, 3, 4, 6, 11–16]). Our data More than 50% of carcinomas had a size between must be evaluated in light of the fact that our inclusion 1 and 5 mm and therefore, the use of thin sections criteria were very strict and selective, for example, we represents a critical factor for early detection of oc- cult carcinoma. In the literature, the histopathologic aspect has not been widely discussed and we have 1% found a considerable heterogeneity in the description 1% of the techniques used. Another factor that can bias 1% the overall incidence is the sampling number. The studies that report a higher incidence of PTC have an- alyzed fewer patients [6, 11, 14, 15]. The authors that, instead, have considered a more numerous cohort re- 28% ported incidences closer to ours [13, 16]. At the histopathological examination, we did not detect follicular cancer or poor differentiated can- cers. All the 89 cases were papillary microcarcinomas, mostly showing a less aggressive variant (classical and follicular); only one case had a more aggressive subtype, the diffuse sclerosing variant, in line with the results reported in the literature [1, 3, 13–20]. 69% In our study the female/male ratio was 3.9:1 (no difference in the incidences of mPTC by χ test), sim- ilar to the results of other recent studies. This finding may be explained by the higher number of diagnos- tic tests performed on women because of the greater prevalence of thyroid benign disease in females [15, 18]. Classical Follicular Mixed Diffuse sclerosing Oncocyc As epidemiologic data, we highlight the association Fig. 1 Histology in patients with mPTC in the series (n = 89) between the incidence of mPTC and non-toxic multin- 130 Incidental thyroid papillary microcarcinoma on 1777 surgically treated patients for benign thyroid disease K original report odular goiter. A few authors have analyzed this associ- in primary operation for benign disease [6, 13]. In ation, with different results [3, 15]. Miccoli et al. found case of uninodular goiter partial thyroidectomy can be a significant difference in the incidence between non- performed: the statistical analysis of our data confirm toxic and toxic disease, with a higher number of ITC that the incidence of ITC in hemythyroidectomy is not in euthyroid patients [1]. Cerci et al. compared the significantly increased to justify total thyroidectomy in incidence of ITC in toxic and non-toxic multinodular these patients. However, considering the above, in our goiter, testing the idea that hyperthyroidism can be opinion it is safer to perform a completion thyroidec- a protective factor, and found a similar incidence of tomy if a mPTC is diagnosed during the histopatho- cancer in the two groups [11]. logical examination, especially in the following: pa- The surgical approach in mPTC is still controver- tients older than 50 years and with familial disposi- sial. Regarding the mPTC diagnosed preoperatively, tion for thyroid cancer; peripheral tumors larger than the 2015 American Thyroid Association guidelines 5 mm and with aggressive variants. suggest active surveillance instead of immediate As the majority of cases with incidental mPTC are surgery for low-risk mPTC [21] and many authors low aggressive variants, we believe total thyroidec- have followed this strategy [22, 23]. tomy without prophylactic central neck dissection is In 2016, Fukuoka et al. suggested active surveil- appropriate, as also suggested by the American guide- lance based on ultrasound criteria, such as calcifica- lines for small, noninvasive and clinically node-neg- tion pattern and vascularization: lesions with stronger ative PTC [21]. Thus, if total thyroidectomy was the calcification and poorer vascularity showed a lower first therapeutic step, we just perform an endocrine tendency to progress [22] Considering risks and ben- and oncologic follow-up. If, however, at first a partial efits of the surgical procedures, in carefully selected thyroidectomy was performed, we suggest a comple- patients, a protocol based on active surveillance with tion thyroidectomy without central neck dissection. periodic checks andultrasoundexaminations can be After surgery, radioiodine ablation is not recom- proposed to low-risk patients [23]. mended in patients with unifocal, low risk carcinoma Even the treatment options for ITC-mPTC are vari- or in the presence of multifocal tumor when the sum able and different. of all the foci is less than 1 cm, and thyroid hormone Some authors, followers of the so-called “Porto therapy should be administered in replacement doses Proposal Criteria” introduced in 2003 by Rosai et al. [21]. [10], continue to support a “conservative” surgical We suggest that after surgery, patients should be approach on the basis of specific characteristics of followed with periodic ultrasound examination of the mPTC: excellent prognosis, low aggressiveness and neck and measurement of serum thyroglobulin. high responsiveness to metabolic radioiodine ther- apy. Take home message Despite the overall excellent prognosis, in the lit- erature mPTC is associated with a 1.0% disease-re- A review of the literature and analysis of our data lated mortality rate, a 5.0% lymph node recurrence showed that mPTC is an important nosologic entity rate, and a 2.5% distant metastasis rate [5]. Therefore, and its management is still controversial. other authors, even taking into account the possibility In our opinion, in case of multinodular non-toxic goi- of multifocality and the risks associated with a second ter, performing total thyroidectomy achieves the best surgery, support total thyroidectomy as the most ac- results regarding the endocrine disease, and also the ceptable procedure [6, 12, 24, 25]. Moreover, total oncologic radicality if a mPTC is discovered. thyroidectomy allows easier follow-up, in particular In case of uninodular goiter, it is appropriate to per- with regard to scintigraphic scan and thyroglobulin form a hemithyroidectomy and if a mPTC is found, we measurement [6]. recommend a completion thyroidectomy, especially The American and European guidelines suggest in determined cases. a conservative approach in patients with unifocal The association between ITC-mPTC and non-toxic mPTC (classic or follicular variant) without extrathy- disease must be further investigated with other stud- roid infiltration and evidence of lymph node metas- ies. tases: a completion thyroidectomy can be avoided in Author Contribution All authors contributed significantly patients treated with lobectomy for benign disease [9, to the present research and reviewed the entire manuscript. 21]. G. Peluso contributed to execution of the study, to the anal- In our university hospital, the surgical approach ysis and interpretation of the data and to the drafting and for multinodular goiter is total thyroidectomy. It can editing of the manuscript. S. Masone reviewed and approved be the procedure of choice because it is safe pro- the final manuscript and performed some of the surgical op- cedure and allows to achieve endocrine control and erations. C. Criscitiello participated in the editing and review complete tumor resection if ITC is discovered, espe- of the manuscript. S. Campanile, C. Dodaro and A. Calogero contributed to the review of the literature. P. Incollingo con- cially considering that the risks for major complica- tributed to the editing of the manuscript and the English tions, (e.g., permanent hypoparathyroidism or recur- language.G.Minieri and M.Menkulazi edited the tables and rent laryngeal injury) are greater in reoperation than K Incidental thyroid papillary microcarcinoma on 1777 surgically treated patients for benign thyroid disease 131 original report the image. A. Scotti, V. Tammaro, A. Jamshidi, L. Pelosio, 9. British Thyroid Association, Royal College of Physicians. M. Caggiano and N. Carlomagno performed some of the sur- British thyroid association guidelines for the management gical operations. M.L. Santangelo contributed to the design of thyroid cancer. 2nd ed. 2007. http://www.british- and the execution of the study, performed some of the surgical thyroidassociation.org/guidelines/. operations, reviewed and approved the final manuscript. 10. Rosai J, Livoisi VA, Sobrinho-Simoes M, et al. 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memo - Magazine of European Medical Oncology – Springer Journals
Published: Mar 31, 2020
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