Thyroid nodules ≤ 1 cm and papillary thyroid microcarcinomas: Brazilian experts opinion

Pedro Weslley Rosario Laura Sterian Ward Hans Graf Fernanda Vaisman Gabriela Franco Mourão Mario Vaisman About the authors

ABSTRACT

The indolent evolution of low-risk papillary thyroid microcarcinoma (mPTC) in adult patients and the consequences of thyroidectomy require a revision of the management traditionally recommended. Aiming to spare patients unnecessary procedures and therapies and to optimize the health system in Brazil, we suggest some measures. Fine-needle aspiration of nodules ≤ 1 cm without extrathyroidal extension on ultrasonography should be performed only in nodules classified as “very suspicious” (i.e., high suspicion according to ATA, high risk according to AACE, TI-RADS 5) and in selected cases [age < 40 years, nodule adjacent to the trachea or recurrent laryngeal nerve (RLN), multiple suspicious nodules, presence of hypercalcitoninemia or suspicious lymph nodes]. Active surveillance (AS) rather than immediate surgery should be considered in adult patients with low-risk mPTC. Lobectomy is the best option in patients with unifocal low-risk mPTC who are not candidates for AS because of age, proximity of the tumor to the trachea or RLN, or because they opted for surgery. The same applies to patients who started AS but had a subsequent surgical indication not due to a suspicion of tumor extension beyond the gland or multicentricity. Molecular tests are not necessary to choose between AS and surgery or, in the latter case, between lobectomy and total thyroidectomy. The presence of RAS or other RAS-like mutations or BRAFV600E or other BRAF V600E-like mutations should not modify the management cited above; however, the rare cases of mPTC exhibiting high-risk mutations, like in the TERT promoter or p53, are not candidates for AS.

Fine needle aspiration; thyroid papillary microcarcinoma; active surveillance; lobectomy

INTRODUCTION

The Brazilian National Institute of Cancer (INCA) estimates an incidence of 1,570 new thyroid tumors in males and 8,040 in females for each year of the 2018-2019 biennium, with an estimated risk of 1.49 and 7.57 cases per 100,000 men and women, respectively (11. Instituto Nacional de Câncer (INCA). Estimativa – 2018. Incidência de Câncer no Brasil. Available at: http://www1.inca.gov.br/estimativa/2018/sintese-de-resultados-comentarios.asp´.
http://www1.inca.gov.br/estimativa/2018/...
). As shown in Table 1, thyroid cancer is the fifth most common tumor in women.

Table 1
INCA estimates of tumors in Brazilian women for 2018-2019

The incidence of thyroid cancer varies considerably across the different regions of Brazil (11. Instituto Nacional de Câncer (INCA). Estimativa – 2018. Incidência de Câncer no Brasil. Available at: http://www1.inca.gov.br/estimativa/2018/sintese-de-resultados-comentarios.asp´.
http://www1.inca.gov.br/estimativa/2018/...
). The incidence is 9.75 cases/100,000 women in well-developed regions such as the southeast, but only 2.8/100,000 among women from the poorer northern part of the country (11. Instituto Nacional de Câncer (INCA). Estimativa – 2018. Incidência de Câncer no Brasil. Available at: http://www1.inca.gov.br/estimativa/2018/sintese-de-resultados-comentarios.asp´.
http://www1.inca.gov.br/estimativa/2018/...
). The remarkable geographic variation and sex disparity in thyroid cancer rates observed across regions may reflect differences in ascertainment, diagnosis, treatment, and death certification of this disease, as well as healthcare access. The same phenomenon has been observed in other Latina American countries (22. Sierra MS, Soerjomataram I, Forman D. Thyroid cancer burden in Central and South America. Cancer Epidemiol. 2016;44(Suppl 1):S150-7.). However, it is noteworthy that mortality rates have remained stable or declined in Brazil, as observed in many other countries, suggesting widespread overdiagnosis (detection of tumors that will not cause clinical illness or death) (33. La Vecchia C, Malvezzi M, Bosetti C, Garavello W, Bertuccio P, Levi F, Negri E. Thyroid cancer mortality and incidence: a global overview. Int J Cancer. 2015;136(9):2187-95.,44. Ahn HS, Kim HJ, Welch HG. Korea’s thyroid-cancer “epidemic” – screening and overdiagnosis. N Engl J Med. 2014;371(19):1765-7.). Even in a study reporting a divergent result, the increase in mortality/100,000 inhabitants per year was lower than the increase in incidence (55. Lim H, Devesa SS, Sosa JA, Check D, Kitahara CM. Trends in Thyroid Cancer Incidence and Mortality in the United States, 1974-2013. JAMA. 2017;317(13):1338-48.). This finding suggests that, even if some actual increase in thyroid cancer cases exists, overdiagnosis is a predominant factor (55. Lim H, Devesa SS, Sosa JA, Check D, Kitahara CM. Trends in Thyroid Cancer Incidence and Mortality in the United States, 1974-2013. JAMA. 2017;317(13):1338-48.,66. Davies L, Morris L, Hankey B. Increases in Thyroid Cancer Incidence and Mortality. JAMA. 2017;318(4):389-90.). It should also be noted that the slight increase in mortality may in part be iatrogenic - an increase in the number of patients undergoing treatment might lead to a small number of treatment-related deaths, or due to attribution bias - the incorrect assignment of the cause of death to cancer in a person’s medical history rather than correctly to other causes (66. Davies L, Morris L, Hankey B. Increases in Thyroid Cancer Incidence and Mortality. JAMA. 2017;318(4):389-90.).

In addition to the very sensitive ultrasound devices that are largely available and accessible to the general population at relatively low cost, new detection techniques now routinely reveal small tumors. These diagnoses may cause anxiety not only in the patient and his family, but also in the physician. The easiest and most practical way to deal with the situation is often immediate surgery. In the case of thyroid tumors, the procedure is often followed by unnecessary and even harmful radioiodine administration. The burden of such interventions has dramatically increased in the past years.

Recent data from South Korea suggest that the epidemic of thyroid tumors observed in that country dramatically dropped to before ultrasound screening levels after a group of physicians, supported by the media, led a campaign against routine screening for thyroid cancer (77. Ahn HS, Welch HG. South Korea’s Thyroid-Cancer “Epidemic” – Turning the Tide. N Engl J Med. 2015;373(24):2389-90.,88. Jung KW, Won YJ, Kong HJ, Lee ES. Prediction of Cancer Incidence and Mortality in Korea, 2018. Cancer Res Treat. 2018;50(2):317-23.). In fact, the United States Preventive Services Task Force (USPSTF) (99. US Preventive Services Task Force, Bibbins-Domingo K, Grossman DC, Curry SJ, Barry MJ, Davidson KW, Doubeni CA, et al. Screening for Thyroid Cancer: US Preventive Services Task Force Recommendation Statement. JAMA. 2017;317(18):1882-7.) and the American Thyroid Association (1010. Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, et al. 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer: The American Thyroid Association Guidelines Task Force on Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid. 2016;26(1):1-133.) advocate against screening for thyroid cancer in asymptomatic adults.

There is an urgent need for a new appraisal of the management of thyroid nodules and tumors. In addition, it is very important to make it clear to patients that immediate interventions and aggressive procedures do not necessarily promote better outcomes and may even not be the best choices.

PAPILLARY THYROID MICROCARCINOMAS

Papillary microcarcinomas are frequently detected during examination of the thyroid in patients who died of unrelated causes and without a history of thyroid malignancy or in patients submitted to thyroidectomy due to benign disease of the gland. This frequency ranges from 1% to 8% in Brazil (1111. Bisi H, Fernandes VS, de Camargo RY, Koch L, Abdo AH, de Brito T. The prevalence of unsuspected thyroid pathology in 300 sequential autopsies, with special reference to the incidental carcinoma. Cancer. 1989;64(9):1888-93.

12. Basílio-De-Oliveira CA. Infectious and neoplastic disorders of the thyroid in AIDS patients: an autopsy study. Braz J Infect Dis. 2000;4(2):67-75.

13. de Matos PS, Ferreira AP, Ward LS. Prevalence of papillary microcarcinoma of the thyroid in Brazilian autopsy and surgical series. Endocr Pathol. 2006;17:165-73.
-1414. Ramos AM, Sales Ade O, Barbalho de Mello LE, Cirino de Andrade M, Pinto Paiva F, Ramos CC, et al. Absence of peritumoral fibrosis or inflammatory infiltrate may be related to clinical progression of papillary thyroid microcarcinoma. Int J Surg Pathol. 2009(6);17:432-7.). Moreover, the prevalence of papillary thyroid carcinoma (PTC) detected by ultrasonographic screening in subjects without a family history of thyroid cancer or a history of radiation exposure, who had no abnormalities upon thyroid palpation, was reported to be 1.2% (1515. Rosario PW, Mineiro Filho AF, Prates BS, Silva LC, Lacerda RX, Calsolari MR. Ultrasonographic screening for thyroid cancer in siblings of patients with apparently sporadic papillary carcinoma. Thyroid. 2012;22(8):805-8.). As observed around the world, an enormous disproportion exists in Brazil between this frequency of “occult” PTC and the number of patients diagnosed with this tumor (11. Instituto Nacional de Câncer (INCA). Estimativa – 2018. Incidência de Câncer no Brasil. Available at: http://www1.inca.gov.br/estimativa/2018/sintese-de-resultados-comentarios.asp´.
http://www1.inca.gov.br/estimativa/2018/...
,1616. Coeli CM, Brito AS, Barbosa FS, Ribeiro MG, Sieiro AP, Vaisman M. [Incidence and mortality from thyroid cancer in Brazil]. Arq Bras Endocrinol Metabol. 2005;49(4):503-9.

17. Cordioli MI, Canalli MH, Coral MH. Increase incidence of thyroid cancer in Florianopolis, Brazil: comparative study of diagnosed cases in 2000 and 2005. Arq Bras Endocrinol Metabol. 2009;53(4):453-60.
-1818. Veiga LH, Neta G, Aschebrook-Kilfoy B, Ron E, Devesa SS. Thyroid cancer incidence patterns in Sao Paulo, Brazil, and the U.S. SEER program, 1997-2008. Thyroid. 2013;23(6):748-57.). Since many of the last cases are currently discovered “incidentally” during imaging examination of asymptomatic individuals without palpable thyroid nodules, this disproportion is even higher if we consider only clinically apparent tumors. This great disparity per se shows that the progression of PTC to a clinically manifest stage occurs only in a small portion of these tumors.

As a confirmation, several studies evaluating the low-risk papillary thyroid microcarcinomas (mPTC) in adults (1919. Ito Y, Miyauchi A, Kihara M, Higashiyama T, Kobayashi K, Miya A. Patient age is significantly related to the progression of papillary microcarcinoma of the thyroid under observation. Thyroid. 2014;24(1):27-34.

20. Sugitani I. Active surveillance for very low-risk papillary thyroid carcinoma: experience and perspectives from Japan. Ann Thyroid. 2018;3:26.

21. Tuttle RM, Fagin JA, Minkowitz G, Wong RJ, Roman B, Patel S, et al. Natural History and Tumor Volume Kinetics of Papillary Thyroid Cancers During Active Surveillance. JAMA Otolaryngol Head Neck Surg. 2017;143(10):1015-20.

22. Sanabria A. Active Surveillance in Thyroid Microcarcinoma in a Latin-American Cohort. JAMA Otolaryngol Head Neck Surg. 2018;144(10):947-8.
-2323. Oh HS, Ha J, Kim HI, Kim TH, Kim WG, Lim DJ, et al. Active Surveillance of Low-Risk Papillary Thyroid Microcarcinoma: A Multi-Center Cohort Study in Korea. Thyroid. 2018;28(12):1587-94.) have shown that tumor growth is uncommon and that the development of apparent lymph node metastases is even rarer. So far there are no reports of the occurrence of distant metastases (Table 2). Curiously, even a reduction of mPTC has been observed in 5% to 15% of patients (2020. Sugitani I. Active surveillance for very low-risk papillary thyroid carcinoma: experience and perspectives from Japan. Ann Thyroid. 2018;3:26.,2121. Tuttle RM, Fagin JA, Minkowitz G, Wong RJ, Roman B, Patel S, et al. Natural History and Tumor Volume Kinetics of Papillary Thyroid Cancers During Active Surveillance. JAMA Otolaryngol Head Neck Surg. 2017;143(10):1015-20.,2424. Ito Y, Uruno T, Nakano K, Takamura Y, Miya A, Kobayashi K, et al. An observation trial without surgical treatment in patients with papillary microcarcinoma of the thyroid. Thyroid. 2003;13(4):381-7.,2525. Kwon H, Oh HS, Kim M, Park S, Jeon MJ, Kim WG, et al. Active Surveillance for Patients With Papillary Thyroid Microcarcinoma: A Single Center’s Experience in Korea. J Clin Endocrinol Metab. 2017;102(6):1917-25.). Regarding the characteristics at the time of diagnosis, patient age has been related to the risk of tumor growth, which is higher in young individuals (1919. Ito Y, Miyauchi A, Kihara M, Higashiyama T, Kobayashi K, Miya A. Patient age is significantly related to the progression of papillary microcarcinoma of the thyroid under observation. Thyroid. 2014;24(1):27-34.

20. Sugitani I. Active surveillance for very low-risk papillary thyroid carcinoma: experience and perspectives from Japan. Ann Thyroid. 2018;3:26.
-2121. Tuttle RM, Fagin JA, Minkowitz G, Wong RJ, Roman B, Patel S, et al. Natural History and Tumor Volume Kinetics of Papillary Thyroid Cancers During Active Surveillance. JAMA Otolaryngol Head Neck Surg. 2017;143(10):1015-20.,2323. Oh HS, Ha J, Kim HI, Kim TH, Kim WG, Lim DJ, et al. Active Surveillance of Low-Risk Papillary Thyroid Microcarcinoma: A Multi-Center Cohort Study in Korea. Thyroid. 2018;28(12):1587-94.). One study also associated serum TSH > 2.5 mIU/L with a higher risk of tumor growth (2626. Kim HI, Jang HW, Ahn HS, Ahn S, Park SY, Oh YL, et al. High Serum TSH Level Is Associated With Progression of Papillary Thyroid Microcarcinoma During Active Surveillance. J Clin Endocrinol Metab. 2018;103(2):446-51.). Importantly, low-risk mPTC is defined in the absence of known distant metastases, apparent extrathyroidal invasion or lymph node involvement, when the tumor is not adjacent to the trachea or recurrent laryngeal nerve, and when fine-needle aspiration (FNA) is not suggestive of an aggressive subtype.

Table 2
Natural history of low-risk papillary thyroid microcarcinoma in adult patients

Even without the adverse effects of radioactive iodine and the risks of exogenous suppression of TSH, therapies no longer recommended for low-risk mPTC (2727. Rosário PW, Ward LS, Carvalho GA, Graf H, Maciel RM, Maciel LM, et al.; Sociedade Brasileira de Endocrinologia e Metabologia. Thyroid nodules and differentiated thyroid cancer: update on the Brazilian consensus. Arq Bras Endocrinol Metabol. 2013;57(4):240-64.) but still prescribed for many patients with this tumor, the undesirable consequences of surgery remain. Although uncommon, hypoparathyroidism and recurrent laryngeal nerve injury can occur even when thyroidectomy is performed by experienced surgeons. Inevitable after total thyroidectomy, levothyroxine replacement therapy is also commonly required in patients with PTC after a lobectomy (2828. Rosário PW, Pereira LF, Borges MA, Alves MF, Purisch S. Factors predicting the occurrence of hypothyroidism after hemithyroidectomy. Thyroid. 2006;16(7):707.,2929. De Carlucci D Jr, Tavares MR, Obara MT, Martins LA, Hojaij FC, Cernea CR. Thyroid function after unilateral total lobectomy: risk factors for postoperative hypothyroidism. Arch Otolaryngol Head Neck Surg. 2008;134(10):1076-9.). The difficulty of achieving sustained control, patient dissatisfaction and compromised quality of life during this lifelong therapy have been shown in a Brazilian multicenter study (3030. Vaisman F, Coeli CM, Ward LS, Graf H, Carvalho G, Montenegro R Jr, et al. How good is the levothyroxine replacement in primary hypothyroidism patients in Brazil? Data of a multicentre study. J Endocrinol Invest. 2013;36(7):485-8.,3131. Vigário P dos S, Vaisman F, Coeli CM, Ward L, Graf H, Carvalho G, et al. Inadequate levothyroxine replacement for primary hypothyroidism is associated with poor health-related quality of life -a Brazilian multicentre study. Endocrine. 2013;44:434-40.).

RECOMMENDATIONS

The low risk of progression and the consequences of surgery, even lobectomy performed by experienced surgeons, are factors that lead to the rethinking of immediate surgery as the best option in patients with low-risk mPTC and that have resulted in the strong current trend of considering active surveillance as the most adequate management in this situation. In clinical practice, three approaches have been adopted to avoid overtreatment of these patients.

First, FNA of nodules ≤ 1 cm without apparent extrathyroidal invasion or lymph node disease on ultrasonography (US), which was already restricted to “very suspicious” nodules, is now only recommended in selected cases or is no longer indicated even in these nodules (Table 3).

Table 3
Recommendation of fine-needle aspiration (FNA) in Europe and the United States for adults with “very suspicious”§ nodules ≤ 1 cm without extrathyroidal extension or lymph node involvement on ultrasonography

Recommendation 1: This panel recommends FNA for nodules ≤ 1 cm if they are “very suspicious” on US and, additionally, if any of the features listed in Table 4 is observed. Obviously, patients initially not submitted to FNA should be monitored and FNA may be indicated during follow-up (Table 4).

Table 4
Fine-needle aspiration (FNA) recommended by this panel for adults with “very suspicious”§ nodules ≤ 1 cm on ultrasonography (US) and follow-up of patients not submitted to FNA

Recommendation 2: In the case of patients submitted to FNA whose result of cytology or molecular testing is compatible with PTC, this panel recommends active surveillance rather than immediate surgery as an option in many cases (Table 5). It is also important to note here that patients initially not submitted to surgery should be followed up closely and thyroidectomy might be indicated later (Table 5).

Table 5
Criteria suggested by this panel for the choice of active surveillance over immediate surgery in adult patients with papillary thyroid microcarcinoma and follow-up of patients not submitted to surgery

One noteworthy finding is the excellent evolution of patients whose surgery was only performed later for several reasons, including tumor progression. Among 303 patients who underwent surgery after a period of active surveillance, highlighting that most of them did not receive radioactive iodine, only one case of short-term local recurrence (0.35%) was observed (1919. Ito Y, Miyauchi A, Kihara M, Higashiyama T, Kobayashi K, Miya A. Patient age is significantly related to the progression of papillary microcarcinoma of the thyroid under observation. Thyroid. 2014;24(1):27-34.

20. Sugitani I. Active surveillance for very low-risk papillary thyroid carcinoma: experience and perspectives from Japan. Ann Thyroid. 2018;3:26.
-2121. Tuttle RM, Fagin JA, Minkowitz G, Wong RJ, Roman B, Patel S, et al. Natural History and Tumor Volume Kinetics of Papillary Thyroid Cancers During Active Surveillance. JAMA Otolaryngol Head Neck Surg. 2017;143(10):1015-20.,2323. Oh HS, Ha J, Kim HI, Kim TH, Kim WG, Lim DJ, et al. Active Surveillance of Low-Risk Papillary Thyroid Microcarcinoma: A Multi-Center Cohort Study in Korea. Thyroid. 2018;28(12):1587-94.), a rate similar to that found in patients operated on immediately after diagnosis.

Recommendation 3: This panel recommends lobectomy as the best option for patients with mPTC who are not candidates for active surveillance because of age, proximity of the tumor to the trachea or recurrent laryngeal nerve, or because they opted for surgery, but who meet the remaining criteria reported in Table 5. The same applies to patients who started active surveillance but had a subsequent surgical indication not due to tumor beyond the gland or multicentricity.

Recently, treatment of mPTC with ablative techniques such as laser, radiofrequency, microwave or percutaneous ethanol injection has been reported (3838. Zhang M, Luo Y, Zhang Y, Tang J. Efficacy and Safety of Ultrasound-Guided Radiofrequency Ablation for Treating Low-Risk Papillary Thyroid Microcarcinoma: A Prospective Study. Thyroid. 2016;26(11):1581-7.

39. Zhang L, Zhou W, Zhan W, Peng Y, Jiang S, Xu S. Percutaneous Laser Ablation of Unifocal Papillary Thyroid Microcarcinoma: Utility of Conventional Ultrasound and Contrast-Enhanced Ultrasound in Assessing Local Therapeutic Response. World J Surg. 2018;42(8):2476-84.

40. Li J, Liu Y, Liu J, Qian L. Ultrasound-guided percutaneous microwave ablation versus surgery for papillary thyroid microcarcinoma. Int J Hyperthermia. 2018;34(5):653-9.
-4141. Jeong SY, Baek JH, Choi YJ, Lee JH. Ethanol and thermal ablation for malignant thyroid tumours. Int J Hyperthermia. 2017;33(8):938-45.). Although studies have demonstrated the short-term efficacy and safety of these procedures, it is the current opinion of this panel that there is no evidence of their superiority over active surveillance in patients who are candidates for the latter, or of their superiority over surgery when it is indicated and feasible.

Recommendation 4: This panel considers that, provided the criteria of Tables 5 and 6 are met, molecular tests are not necessary to choose between active surveillance and surgery or, in the latter case, between lobectomy and total thyroidectomy. In cases in which molecular tests are obtained, the presence of RAS or other RAS-like mutations (e.g., PAX8/PPARG rearrangement) or BRAFV600E or other BRAF V600E-like mutations (e.g., RET/PTC fusions) should not modify the management cited above. Mutations in the TERT promoter were recently reported to correlate strongly with aggressiveness in advanced forms of thyroid cancer. Although they are uncommon in mPTC apparently restricted to the thyroid (4343. de Biase D, Gandolfi G, Ragazzi M, Eszlinger M, Sancisi V, Gugnoni M, et al. TERT Promoter Mutations in Papillary Thyroid Microcarcinomas. Thyroid. 2015;25(9):1013-9.) and have not been associated with the growth or development of lymph node metastases in mPTC under active surveillance (4444. Yabuta T, Matsuse M, Hirokawa M, Yamashita S, Mitsutake N, Miyauchi A. TERT Promoter Mutations Were Not Found in Papillary Thyroid Microcarcinomas That Showed Disease Progression on Active Surveillance. Thyroid. 2017;27(9):1206-7.), this panel currently considers that the rare cases of mPTC exhibiting high-risk mutations, like in the TERT promoter or p53, are not candidates for active surveillance.

Table 6
Criteria suggested by this panel for the choice of lobectomy in patients with papillary microcarcinoma and for the indication of surgical complementation in the short-term.

REFERENCES

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  • 4
    Ahn HS, Kim HJ, Welch HG. Korea’s thyroid-cancer “epidemic” – screening and overdiagnosis. N Engl J Med. 2014;371(19):1765-7.
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    Lim H, Devesa SS, Sosa JA, Check D, Kitahara CM. Trends in Thyroid Cancer Incidence and Mortality in the United States, 1974-2013. JAMA. 2017;317(13):1338-48.
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    Davies L, Morris L, Hankey B. Increases in Thyroid Cancer Incidence and Mortality. JAMA. 2017;318(4):389-90.
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    Ahn HS, Welch HG. South Korea’s Thyroid-Cancer “Epidemic” – Turning the Tide. N Engl J Med. 2015;373(24):2389-90.
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    Jung KW, Won YJ, Kong HJ, Lee ES. Prediction of Cancer Incidence and Mortality in Korea, 2018. Cancer Res Treat. 2018;50(2):317-23.
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    US Preventive Services Task Force, Bibbins-Domingo K, Grossman DC, Curry SJ, Barry MJ, Davidson KW, Doubeni CA, et al. Screening for Thyroid Cancer: US Preventive Services Task Force Recommendation Statement. JAMA. 2017;317(18):1882-7.
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    Bisi H, Fernandes VS, de Camargo RY, Koch L, Abdo AH, de Brito T. The prevalence of unsuspected thyroid pathology in 300 sequential autopsies, with special reference to the incidental carcinoma. Cancer. 1989;64(9):1888-93.
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    Basílio-De-Oliveira CA. Infectious and neoplastic disorders of the thyroid in AIDS patients: an autopsy study. Braz J Infect Dis. 2000;4(2):67-75.
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    de Matos PS, Ferreira AP, Ward LS. Prevalence of papillary microcarcinoma of the thyroid in Brazilian autopsy and surgical series. Endocr Pathol. 2006;17:165-73.
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    Ramos AM, Sales Ade O, Barbalho de Mello LE, Cirino de Andrade M, Pinto Paiva F, Ramos CC, et al. Absence of peritumoral fibrosis or inflammatory infiltrate may be related to clinical progression of papillary thyroid microcarcinoma. Int J Surg Pathol. 2009(6);17:432-7.
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    Rosario PW, Mineiro Filho AF, Prates BS, Silva LC, Lacerda RX, Calsolari MR. Ultrasonographic screening for thyroid cancer in siblings of patients with apparently sporadic papillary carcinoma. Thyroid. 2012;22(8):805-8.
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    Coeli CM, Brito AS, Barbosa FS, Ribeiro MG, Sieiro AP, Vaisman M. [Incidence and mortality from thyroid cancer in Brazil]. Arq Bras Endocrinol Metabol. 2005;49(4):503-9.
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    Cordioli MI, Canalli MH, Coral MH. Increase incidence of thyroid cancer in Florianopolis, Brazil: comparative study of diagnosed cases in 2000 and 2005. Arq Bras Endocrinol Metabol. 2009;53(4):453-60.
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    Veiga LH, Neta G, Aschebrook-Kilfoy B, Ron E, Devesa SS. Thyroid cancer incidence patterns in Sao Paulo, Brazil, and the U.S. SEER program, 1997-2008. Thyroid. 2013;23(6):748-57.
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    Ito Y, Miyauchi A, Kihara M, Higashiyama T, Kobayashi K, Miya A. Patient age is significantly related to the progression of papillary microcarcinoma of the thyroid under observation. Thyroid. 2014;24(1):27-34.
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    Sugitani I. Active surveillance for very low-risk papillary thyroid carcinoma: experience and perspectives from Japan. Ann Thyroid. 2018;3:26.
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    Tuttle RM, Fagin JA, Minkowitz G, Wong RJ, Roman B, Patel S, et al. Natural History and Tumor Volume Kinetics of Papillary Thyroid Cancers During Active Surveillance. JAMA Otolaryngol Head Neck Surg. 2017;143(10):1015-20.
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    Sanabria A. Active Surveillance in Thyroid Microcarcinoma in a Latin-American Cohort. JAMA Otolaryngol Head Neck Surg. 2018;144(10):947-8.
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    Oh HS, Ha J, Kim HI, Kim TH, Kim WG, Lim DJ, et al. Active Surveillance of Low-Risk Papillary Thyroid Microcarcinoma: A Multi-Center Cohort Study in Korea. Thyroid. 2018;28(12):1587-94.
  • 24
    Ito Y, Uruno T, Nakano K, Takamura Y, Miya A, Kobayashi K, et al. An observation trial without surgical treatment in patients with papillary microcarcinoma of the thyroid. Thyroid. 2003;13(4):381-7.
  • 25
    Kwon H, Oh HS, Kim M, Park S, Jeon MJ, Kim WG, et al. Active Surveillance for Patients With Papillary Thyroid Microcarcinoma: A Single Center’s Experience in Korea. J Clin Endocrinol Metab. 2017;102(6):1917-25.
  • 26
    Kim HI, Jang HW, Ahn HS, Ahn S, Park SY, Oh YL, et al. High Serum TSH Level Is Associated With Progression of Papillary Thyroid Microcarcinoma During Active Surveillance. J Clin Endocrinol Metab. 2018;103(2):446-51.
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    Rosário PW, Ward LS, Carvalho GA, Graf H, Maciel RM, Maciel LM, et al.; Sociedade Brasileira de Endocrinologia e Metabologia. Thyroid nodules and differentiated thyroid cancer: update on the Brazilian consensus. Arq Bras Endocrinol Metabol. 2013;57(4):240-64.
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    Rosário PW, Pereira LF, Borges MA, Alves MF, Purisch S. Factors predicting the occurrence of hypothyroidism after hemithyroidectomy. Thyroid. 2006;16(7):707.
  • 29
    De Carlucci D Jr, Tavares MR, Obara MT, Martins LA, Hojaij FC, Cernea CR. Thyroid function after unilateral total lobectomy: risk factors for postoperative hypothyroidism. Arch Otolaryngol Head Neck Surg. 2008;134(10):1076-9.
  • 30
    Vaisman F, Coeli CM, Ward LS, Graf H, Carvalho G, Montenegro R Jr, et al. How good is the levothyroxine replacement in primary hypothyroidism patients in Brazil? Data of a multicentre study. J Endocrinol Invest. 2013;36(7):485-8.
  • 31
    Vigário P dos S, Vaisman F, Coeli CM, Ward L, Graf H, Carvalho G, et al. Inadequate levothyroxine replacement for primary hypothyroidism is associated with poor health-related quality of life -a Brazilian multicentre study. Endocrine. 2013;44:434-40.
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Publication Dates

  • Publication in this collection
    02 Sept 2019
  • Date of issue
    Sep-Oct 2019

History

  • Received
    18 Nov 2018
  • Accepted
    19 June 2019
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