Abstract
Background
This paper aims to review controversies in the management of minimally invasive follicular thyroid carcinoma (MIFTC) and to reach an evidence-based consensus.
Method
MEDLINE search of the literature was conducted using keywords related to MIFTC. The search term was identified in the title, abstract, or medical subject heading. Available literature meeting the inclusion criteria were assigned the appropriate levels of evidence and recommendations in accordance with accepted international standards. Results were discussed at the 2013 Workshop of the European Society of Endocrine Surgeons devoted to MIFTC.
Results
Published papers on MIFTC present inadequate power with a III–IV level of evidence and C grade of recommendation. Several issues demanded a comparison of published studies from different medical reports regarding MIFTC definition, specimen processing, characteristics, diagnosis, prognoses, and therapy. As a consequence, it is difficult to make valuable statements on MIFTC with a sufficient recommendation rating. MIFTC diagnosis requires clearer, unequivocal, and reproducible criteria for pathologist, surgeons, and endocrinologists to use in the management of these patients. If the distinction between MIFTC and WIFTC cannot be made, an expert in thyroid pathologist should be consulted.
Conclusion
According to published papers, the following conclusions can be drawn. (a) Candidates for hemithyroidectomy are MIFTC with exclusive capsular invasion, patients <45 years old at presentation, tumor size <40 mm, without vascular invasion, and without any node or distant metastases. (b) Candidates for total thyroidectomy are MIFTC in patients ≥45 years at presentation, tumor size ≥40 mm, vascular invasion present, positive nodes, and positive distant metastases. (c) In the absence of clinical evidence for lymph node metastasis, patients with MIFTC do not require prophylactic lymph node dissection. (d) Radio iodine ablation is indicated in elderly patients (>45 years), large tumor size (>40 mm), extensive vascular invasion, presence of distant synchronous or metachronous metastasis, positive nodes, and if recurrence is noted at follow-up.
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References
Asari R, Koperek O, Scheuba C, Riss P, Kaserer K, Hoffmann M, Niederle B (2009) Follicular thyroid carcinoma in an iodine-replete endemic goiter region: a prospectively collected, retrospectively analyzed clinical trial. Ann Surg 249(6):1023–1031
Machens A, Holzhausen HJ, Dralle H (2005) The prognostic value of primary tumor size in papillary and follicular thyroid carcinoma. Cancer 103(11):2269–2273
Graham AR (1924) Malignant epithelial tumors of the thyroid with special reference to invasion of blood vessels. Surg Gynecol Obstet 42:781–790
DeLellis RA, Lloyd RV, Heitz PU, Eng C (2004) WHO classification of tumours. Pathology and genetics of tumours of endocrine organs. IARC Press, Lyon, pp 73–76
Fransilla KO, Ackerman LC, Brown CL, Hedinger CE (1985) Follicular carcinoma. Sem Diagn Pathol 2:101–122
Hedinger CE, Williams ED, Sobin LH (1988) Histological typing of thyroid tumours. In: Hedinger CE (ed) International histological classification of tumours, vol 11. Springer, Berlin, pp 7–68
Huang CC, Hsueh C, Liu FH, Chao TC, Lin JD (2011) Diagnostic and therapeutic strategies for minimally and widely invasive follicular thyroid carcinomas. Surg Oncol 20(1):1–6
Goffredo P, Cheung K, Roman SA, Sosa JA (2013) Can minimally invasive follicular thyroid cancer be approached as a benign lesion? A population-level analysis of survival among 1,200 patients. Ann Surg Oncol 20(3):767–772
Hermann M, Tonninger K, Kober F, Furtlehner EM, Schultheis A, Neuhold N (2010) Minimally invasive follicular thyroid carcinoma: not always total thyroidectomy. Chirurg 81(7):627–630, 632–5
Schmid KW, Sheu SY, Görges R, Ensinger C, Tötsch M (2003) Thyroid tumors. Pathologe 24:357–372
Schmid KW, Farid NR (2006) How to define follicular thyroid carcinoma? Virchows Arch 448:385–393
Baloch ZW, Livolsi VA (2002) Pathology of the thyroid gland. In: Livolsi VA, Asa SL (eds) Endocrine pathology. Churchill Livingstone, New York, pp 61–88
Thompson LD, Wieneke JA, Paal E, Frommelt RA, Adair CF, Heffess CS (2001) A clinicopathologic study of minimally invasive follicular carcinoma of the thyroid gland with a review of the English literature. Cancer 91(3):505–524
Agency for Health Care Policy and Research (1992) Acute pain management: operative or medical procedures and trauma. Clinical practice guideline number 1. AHCPR, Rockville, p 107
Agency for Health Care Policy and Research (1994) Management of cancer pain: adults. Clinical practice guideline number 9. AHCPR, Rockville
Van Heerden JA, Hay ID, Goellner JR, Salomao D, Ebersold JR, Bergstralh EJ, Grant CS (1992) Follicular thyroid carcinoma with capsular invasion alone: a non-threatening malignancy. Surgery 112:1130–1136
Kahn NF, Perzin K (1983) Follicular carcinoma of the thyroid. Pathol Annu 18:221–253
Schmid KW, Totsch M, Ofner D, Bocker W, Ladurner D (1997) Minimally invasive follicular thyroid carcinoma: a clinicopathological study. Curr Top Pathol 91:37–43
Meissner WA, Warren S (1968) Atlas of tumor pathology. Tumors of the thyroid gland. Armed Forces Institute of Pathology, Washington, pp 84–95
Delbridge L, Parkyn R, Philips J, Barraclough B, Robinson B (2002) Minimally invasive follicular thyroid carcinoma: completion thyroidectomy or not? ANZ J Surg 72(11):844–845
Rosai J, Carcangiu ML, DeLellis RA (1992) Tumours of the thyroid gland. In: Rosai J, Sobin LH (eds) Atlas of tumor pathology 3rd series, fascicle 5. Armed Forces Institute of Pathology , Washington, pp 49–63
D'Avanzo A, Ituarte P, Treseler P, Kebebew E, Wu J, Wong M, Duh QY, Siperstein AE, Clark OH (2004) Prognostic scoring systems in patients with follicular thyroid cancer: a comparison of different staging systems in predicting the patient outcome. Thyroid 14:453–458
D'Avanzo A, Treseler P, Ituarte PH, Wong M, Streja L, Greenspan FS, Siperstein AE, Duh QY, Clark OH (2004) Follicular thyroid carcinoma: histology and prognosis. Cancer 100:1123–1129
Lo CY, Chan WF, Lam KY, Wan KY (2005) Follicular thyroid carcinoma. The role of histology and staging systems in predicting survival. Ann Surg 242:708–715
Lang BH, Lo CY, Chan WF, Lam KY, Wan KY (2007) Staging systems for follicular thyroid carcinoma: application to 171 consecutive patients treated in a tertiary referral centre. Endocr Relat Cancer 14:29–42
Ghossein R (2009) Update to the College of American Pathologist reporting on thyroid carcinomas. Head Neck Pathol 3(1):86–93
Rosai J (2005) Handling of thyroid follicular patterned lesions. Endocr Pathol 6:279–284
Williams ED (2000) Two proposals regarding the terminology of thyroid tumors. Int J Surg Pathol 8:181–183
Bareck E, Hermann M, Neuhold N et al. (2010) Maligne Tumore der Schilddrüse – Manual der ACO-ASSO (Arbeitsgemeinschaft Chirurgische Onkologie der Österreichischen Gesellschaft für Chirurgie)
Heffess CS, Thompson LD (2001) Minimally invasive follicular thyroid carcinoma. Endocr Pathol 12:417–422
Hirokawa M, Carney JA, Goellner JR, DeLellis RA, Heffess CS, Katoh R, Tsujimoto M, Kakudo K (2002) Observer variation of encapsulated follicular lesions of the thyroid gland. Am J Surg Pathol 16:1508–1514
Goldstein NS, Czako P, Neill JS (2000) Metastatic minimally invasive (encapsulated) follicular and Hurthle cell thyroid carcinoma: a study of 34 patients. Mod Pathol 13:123–130
Lang W, Choritz H, Hundeshagen H (1986) Risk factors in follicular thyroid carcinomas. A retrospective follow-up study covering a 14-year period with emphasis on morphological findings. Am J Surg Pathol 10:246–255
Sugino K, Kameyama K, Ito K, Nagahama M, Kitagawa W, Shibuya H, Ohkuwa K, Yano Y, Uruno T, Akaishi J, Suzuki A, Masaki C, Ito K (2012) Outcomes and prognostic factors of 251 patients with minimally invasive follicular thyroid carcinoma. Thyroid 22(8):798–804
Ito Y, Hirokawa M, Masuoka H, Yabuta T, Kihara M, Higashiyama T, Takamura Y, Kobayashi K, Miya A, Miyauchi A (2013) Prognostic factors of minimally invasive follicular thyroid carcinoma: extensive vascular invasion significantly affects patient prognosis. Endocr J
Ban EJ, Andrabi A, Grodski S, Yeung M, McLean C, Serpell J (2012) Follicular thyroid cancer: minimally invasive tumours can give rise to metastases. ANZ J Surg 82(3):136–139
Collini P, Sampietro G, Rosai J, Pilotti S (2003) Minimally invasive (encapsulated) follicular carcinoma of the thyroid gland is the low-risk counterpart of widely invasive follicular carcinoma but not of insular carcinoma. Virchows Arch 442(1):71–76
Collini P, Sampietro G, Pilotti S (2004) Extensive vascular invasion is a marker of risk of relapse in encapsulated non-Hürthle cell follicular carcinoma of the thyroid gland: a clinicopathological study of 18 consecutive cases from a single institution with a 11-year median follow-up. Histopathology Jan 44(1):35–39
Lang W, Georgii A, Stauch G, Kienzle E (1980) The differentiation of atypical adenomas and encapsulated follicular carcinomas in the thyroid gland. Virchows Arch A Pathol Anat Histol 385:125–141
Franc B, De La Salmoniere P, Lange F, Hoang C, Louvel A, de Roquancourt A, Vildé F, Hejblum G, Chevret S, Chastang C (2003) Interobserver and intraobserver reproducibility in the histopathology of follicular thyroid carcinoma. Hum Pathol 34:1092–1100
Ghossein RA, Hiltzik DH, Carlson DL, Patel S, Shaha A, Shah JP, Tuttle RM, Singh B (2006) Prognostic factors of recurrence in encapsulated Hurthle cell carcinoma of the thyroid gland: a clinicopathologic study of 50 cases. Cancer 106:1669–1676
LiVolsi VD (1993) Pathobiology of the parathyroid and thyroid gland. Lippincott Williams & Wilkins, Baltimore
Grossman RE, Clark O (1997) Hurthle cell carcinoma. Cancer Control 4:13–17
Grebe SK, Hay I (1995) Follicular thyroid cancer. Endocrinol Metab Clin North Am 24:761–801
LiVolsi V (1994) The demise of follicular carcinoma of the thyroid gland. Thyroid 4:233–236
Chow SM, Law SC, Mendenhall WM, Au SK, Yau S, Yuen KT, Law CC, Lau WH (2002) Follicular thyroid carcinoma: prognostic factors and the role of radioiodine. Cancer 95(3):488–498
Clark RM, Rosen IB, Laperierre NJ (1982) Malignant tumors of the head and neck in a young population. Am J Surg 144:459–462
Hogan AR, Zhuge Y, Perez EA, Koniaris LG, Lew JI, Sola JE (2009) Pediatric thyroid carcinoma: incidence and outcomes in 1753 patients. J Surg Res 156:167–172
Balachandar S, Rivera M, LaQuaglia M, Tuttle RM, Sklar C, Ghossein R (2013) Pediatric thyroid carcinomas of follicular cell origin: a clinic–pathologic study of 42 cases. Mod Pathol 26:2
Thompson GB, Hay ID (2004) Current strategies for surgical management and adjuvant treatment of childhood papillary thyroid carcinoma. World J Surg 28:1187–1198
Hay ID, Gonzalez-Losada T, Reinalda MS, Honetschlager JA, Richards ML, Thompson GB (2010) Longterm outcome in 215 children and adolescents with papillary thyroid cancer treated during 1940 through 2008. World J Surg 34:1192–1202
O'Gorman CS, Hamilton J, Rachmiel M, Gupta A, Ngan BY, Daneman D (2010) Thyroid cancer in childhood: a retrospective review of childhood course. Thyroid 20:375–380
Waguespack SG, Francis G (2010) Initial management and follow-up of differentiated thyroid cancer in children. J Natl Compr Canc Netw 8:1289–1300
Landau D, Vini L, A'Hern R, Harmer C (2000) Thyroid cancer in children: the Royal Marsden Hospital experience. Eur J Cancer 36:214–220
Jarzab B, Handkiewicz-Junak D, Wloch J (2005) Juvenile differentiated thyroid carcinoma and the role of radioiodine in its treatment: a qualitative review. Endocr-Relat Cancer 12:773–803
Luster M, Lassmann M, Freudenberg LS, Reiners C (2007) Thyroid cancer in childhood: management strategy, including dosimetry and long-term results. Hormones (Athens) 6:269–278
Clerici T, Kolb W, Beutner U, Bareck E, Dotzenrath C, Kull C, Niederle B (2010) German Association of Endocrine Surgeons. Diagnosis and treatment of small follicular thyroid carcinomas. Br J Surg 97:839–844
Scheiden R, Keipes M, Bock C, Dippel W, Kieffer N, Capesius C (2006) Thyroid cancer in Luxembourg: a national population-based data report (1983–1999). BMC Cancer 6:102
Gritzmann N, Koischwitz D, Rettenbacher T (2000) Sonography of the thyroid and parathyroid glands. Radiol Clin North Am 38:1131–1145
Fukunari N (1998) The role of ultrasonography and color Doppler sonography in the diagnosis of thyroid disease. Thyroidol Clin Exp 10:97–101
Miyakawa M, Onoda N, Etoh M, Fukuda I, Takano K, Okamoto T, Obara T (2005) Diagnosis of thyroid follicular carcinoma by the vascular pattern and velocimetric parameters using high resolution pulsed and power Doppler ultrasonography. Endocr J 52:207–212
Shin JH, Han BK, Ko EY, Oh YL, Kim JH (2010) Differentiation of widely invasive and minimally invasive follicular thyroid carcinoma with sonography. Eur J Radiol 74(3):453–457
Leteurtre E, Leroy X, Pattou F, Wacrenier A, Carnaille B, Proye C, Lecomte-Houcke M (2001) Why do frozen sections have limited value in encapsulated or minimally invasive follicular carcinoma of the thyroid? Am J Clin Pathol 115:370–374
Dralle H, Musholt TJ, Schabram J, Steinmüller T, Frilling A, Simon D, Goretzki PE, Niederle B, Scheuba C, Clerici T, Hermann M, Kußmann J, Lorenz K, Nies C, Schabram P, Trupka A, Zielke A, Karges W, Luster M, Schmid KW, Vordermark D, Schmoll HJ, Mühlenberg R, Schober O, Rimmele H, Machens A (2013) German Association of Endocrine Surgeons practice guideline for the surgical management of malignant thyroid tumors. Langenbecks Arch Surg 398:347–375
LiVolsi VA, Balch ZW (2009) The many faces of follicular variant of papillary thyroid carcinoma. Pathol Case Rev 14:214–218
Chen H, Nicol TL, Udelsman R (1995) Follicular lesions of the thyroid. Does frozen section evaluation alter operative management? Ann Surg 222:101–106
Udelsman R, Westra WH, Donovan PI, Sohn TA, Cameron JL (2001) Randomized prospective evaluation of frozen-section analysis for follicular neoplasms of the thyroid. Ann Surg 233:716–722
Miller MC, Rubin CJ, Cunnane M, Bibbo M, Miller JL, Keane WM, Pribitkin EA (2007) Intraoperative pathologic examination: cost effectiveness and clinical value in patients with cytologic diagnosis of cellular follicular thyroid lesion. Thyroid 17:557–565
Basolo F, Ugolini C, Proietti A, Iacconi P, Berti P, Miccoli P (2007) Role of frozen section associated with intraoperative cytology in comparison to FNA and FS alone in the management of thyroid nodules. Eur J Surg Oncol 33:769–775
Lin HS, Komisar A, Opher E, Blaugrund SM (2000) Follicular variant of papillary carcinoma: the diagnostic limitations of preoperative fine-needle aspiration and intraoperative frozen section evaluation. Laryngoscope 110:1431–1436
Baloch Z, LiVolsi VA, Jain R, Aljada I, Mandel S, Langer JE, Gupta PK (2003) Role of repeat fineneedle aspiration biopsy (FNAB) in the management of thyroid nodules. Diagn Cytopathol 29:203–206
Dosen D, Turic M, Smalcelj J, Janusić R, Grgić MP, Separović V (2003) The value of frozen section in intraoperative surgical management of thyroid follicular carcinoma. Head Neck 25:521–528
Doherty GM (2005) Follicular neoplasms of the thyroid. In: Clark O, Duh Q, Kebebew E (eds) Textbook of endocrine surgery, 2nd edn. Elsevier Saunders, Philadelphia, pp 115–122
Cady B, Rossi R, Slverman M, Wool M (1985) Further evidence of the validity of risk group definition in differentiated thyroid carcinoma. Surgery 98:1171–1178
Harness JK, Thompson NW, McLeod MK, Eckhauser FE, Lloyd RV (1984) Follicular carcinoma of the thyroid gland: trends and treatment. Surgery 96(6):972–980
Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Pacini F, Schlumberger M, Sherman SI, Steward DL, Tuttle RM (2009) Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated cancer. Thyroid 19(11):1167–1214
Gemsenjäger E, Heitz PU, Martina B (1997) Selective treatment of differentiated thyroid carcinoma. World J Surg 21:546–552
Iwasaki H, Matsumoto A, Ito K, Kure Y, Suzuki A, Sugino K, Ozaki O, Noh J (1990) Prediction of distant metastasis in follicular adenocarcinoma of the thyroid. World J Surg 14:425–430
Mazzaferri EL, Jhiang SM (1994) Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med 97:418–428
Mizukami Y, Nonomura A, Hayashi Y, Ohmura K, Michigishi T, Noguchi M, Nakamura S, Ishizaki T (1996) Case report, late bone metastasis from an encapsulated follicular carcinoma of the thyroid without capsular and vascular invasion. Pathol Intl 46:457–461
Dralle H, Lorenz K, Machens A (2009) Chirurgie der Schilddrüsenkarzinome. Chirurg 80:1069–1083
Durante C, Haddy N, Baudin E, Leboulleux S, Hartl D, Travagli JP, Caillou B, Ricard M, Lumbroso JD, De Vathaire F, Schlumberger M (2006) Long-term outcome of 444 patients with distant metastases from papillary and follicular thyroid carcinoma: benefits and limits of radioiodine therapy. J Clin Endocrinol Metab 91:2892–2899
Pacini F, Schlumberger M, Dralle H, Elisei R, Smit JW, Wiersinga W, European Thyroid Cancer Taskforce (2006) European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. Eur J Endocrinol 154:787–803
Shaha AR, Loree TR, Shah JP (1995) Prognostic factors and risk group analysis in follicular carcinoma of the thyroid. Surgery 118:1131–1138
Steinmüller T, Klupp J, Wenking S, Neuhaus P (1999) Complications associated with different surgical approaches to differentiated thyroid carcinoma. Langenbecks Arch Surg 384:50–53
Steinmüller T, Klupp J, Rayes N, Ulrich F, Jonas S, Gräf KJ, Neuhaus P (2000) Prognostic factors in patients with differentiated thyroid carcinoma. Eur J Surg 166:29–33
Alfalah H, Cranshaw I, Jany T, Arnalsteen L, Leteurtre E, Cardot C, Pattou F, Carnaille B (2008) Risk factors for lateral cervical lymph node involvement in follicular thyroid carcinoma. World J Surg 32:2623–2626
Furtlehner E, Schultheis A, Kober F et al. (2010) Evaluation of lymphadenectomy in minimally invasive follicular thyroid carcinoma—time to adapt guidelines. Eur Surg 41 (Suppl 230):230–231
Sawka AM, Brierley JD, Tsang RW, Thabane L, Rotstein L, Gafni A, Straus S, Goldstein DP (2008) An updated systematic review and commentary examining the effectiveness of radioactive iodine remnant ablation in welldifferentiated thyroid cancer. Endocrinol Metab Clin North Am 37:457–480
Jonklaas J, Sarlis NJ, Litofsky D, Ain KB, Bigos ST, Brierley JD, Cooper DS, Haugen BR, Ladenson PW, Magner J, Robbins J, Ross DS, Skarulis M, Maxon HR, Sherman SI (2006) Outcomes of patients with differentiated thyroid carcinoma following initial therapy. Thyroid 16:1229–1242
Ito Y, Hirokawa M, Higashiyama T, Takamura Y, Miya A, Kobayashi K, Matsuzuka F, Kuma K, Miyauchi A (2007) Prognosis and prognostic factors of follicular carcinoma in Japan: importance of postoperative pathological examination. World J Surg 31:1417–1424, 10
Dralle H, Machens A (2008) Surgical approaches in thyroid cancer and lymph node metastases. Best Pract Res Clin Endocrinol Metab 22:971–987
Gilliland FD, Hunt WC, Morris DM, Key CR (1997) Prognostic factors for thyroid carcinoma. A population-based study of 15,698 cases from the Surveillance, Epidemiology and End Results (SEER) program 1973–1991. Cancer 79:564–573
Feldt-Rasmussen U (2001) Iodine and Cancer. Thyroid 11:483–486
Bakiri F, Djemli FK, Mokrane LA, Djidel FK (1998) The relative roles of endemic goiter and socioeconomic development status in the prognosis of thyroid carcinoma. Cancer 82:1146–1153
Brennan MD, Bergstralh EJ, van Heerden JA, McConahey WM (1991) Follicular thyroid cancer treated at the Mayo Clinic, 1946 through 1970: initial manifestations, pathologic findings, therapy, and outcome. Mayo Clin Proc 66:11–22
Passler C, Scheuba C, Prager G, Kaczirek K, Kaserer K, Zettinig G, Niederle B (2004) Prognostic factors of papillary and follicular thyroid cancer: differences in an iodine-replete endemic goiter region. Endocr Relat Cancer 11:131–139
Rivera M, Tuttle RM, Patel S, Shaha A, Shah JP, Ghossein RA (2009) Encapsulated papillary thyroid carcinoma: a clinico-pathologic study of 106 cases with emphasis on its morphologic subtypes (histologic growth pattern). Thyroid 19:119–127
Saadi H, Kleidermacher P, Esselstyn C Jr (2001) Conservative management of patients with intrathyroidal well-differentiated follicular thyroid carcinoma. Surg 130:119–120
Emerick GT, Duh QY, Siperstein AE, Burrow GN, Clark OH (1993) Diagnosis, treatment and outcome of follicular thyroid carcinoma. Cancer 72:3287–3295
Jorda M, Gonzales-Campora R, Mora J, Herrero-Zapatero A, Otal C, Galera H (1993) Prognostic factors in follicular carcinoma of the thyroid. Arch Pathol Lab Med 117:631–635
Warren S (1931) Significance of invasion of blood vessels in adenomas of the thyroid gland. Arch Pathol 11:255–257
O'Neill CJ, Vaughan L, Learoyd DL, Sidhu SB, Delbridge LW, Sywak MS (2011) Management of follicular thyroid carcinoma should be individualised based on degree of capsular and vascular invasion. Eur J Surg Oncol 37:181–185
Nishiyama RH (2005) Pathology of tumors of the thyroid gland. In: Clark O, Duh Q, Kebebew E (eds) Textbook of endocrine surgery, 2nd end. Elsevier Saunders, Philadelphia, pp 223–239
Hamming JF, Roukema JA (2005) Management of regional lymph nodes in papillary, follicular, and medullary thyroid cancer. In: Clark O, Duh Q, Kebebew E (eds) Textbook of endocrine surgery, 2nd edn. Elsevier Saunders, Philadelphia, pp 195–206
Cady B, Rossi R (1988) An expanded view of risk-group definition in differentiated thyroid carcinoma. Surgery 104:947–953
Schelfhout LJ, Creutzberg CL, Hamming JF, Fleuren GJ, Smeenk D, Hermans J, van de Velde CJ, Goslings BM (1988) Multivariate analysis of survival in differentiated thyroid cancer: the prognostic significance of the age factor. Eur J Cancer Clin Oncol 24:331–337
Simpson WJ, McKinney SE, Carruthers JS, Gospodarowicz MK, Sutcliffe SB, Panzarella T (1987) Papillary and follicular thyroid cancer. Prognostic factors in 1578 patients. Am J Med 83:479–488
Besic N, Zgajnar J, Hocevar M, Frkovic-Grazio S (2005) Is patient's age a prognostic factor for follicular thyroid carcinoma in the TNM classification system? Thyroid 15:439–448
Franssila KO, Ackerman LV, Brown CL, Hedinger CE (1985) Follicular carcinoma. Semin Diagn Pathol 2:101–122
Frazell EL, Duffy BJ Jr (1951) Hurthle-cell cancer of the thyroid; a review of forty cases. Cancer 4:952–956
Haigh PI, Urbach DR (2005) The treatment and prognosis of Hurthle cell follicular thyroid carcinoma compared with its non-Hurthle cell counterpart. Surgery 138:1152–1158
Baloch ZW, LiVolsi VA (2000) Encapsulated follicular variant of papillary thyroid carcinoma with bone metastases. Mod Pathol 13:861–865
Carcangiu ML, Zampi G, Rosai J (1984) Poorly differentiated (“insular”) thyroid carcinoma. A reinterpretation of Langhans' “wuchernde Struma”. Am J Surg Pathol 8:655–668
Castro P, Rebocho AP, Soares RJ, Magalhães J, Roque L, Trovisco V, Vieira de Castro I, Cardoso-de-Oliveira M, Fonseca E, Soares P, Sobrinho-Simões M (2006) PAX8-PPARgamma rearrangement is frequently detected in the follicular variant of papillary thyroid carcinoma. J Clin Endocrinol Metab 91:213–220
Chan JKC (2007) Tumors of the thyroid and parathyroid glands. In: Fletcher CDM (ed) Diagnostic histopathology of tumors, vol 2, Chap. 18, 3rd edn. Churchill Livingstone, London, pp 997–1079
Cheung CC, Ezzat S, Freeman JL, Rosen IB, Asa SL (2001) Immunohistochemical diagnosis of papillary thyroid carcinoma. Mod Pathol 14:338–342
Couto JP, Prazeres H, Castro P, Lima J, Máximo V, Soares P, Sobrinho-Simões M (2009) How molecular pathology is changing and will change the therapeutics of patients with follicular cell-derived thyroid cancer. J Clin Pathol 62:414–421
Cvejic DS, Savin SB, Petrovic IM, Paunovic IR, Tatic SB, Havelka MJ (2005) Galectin-3 expression in papillary thyroid carcinoma: relation to histomorphologic growth pattern, lymph node metastasis, extrathyroid invasion, and tumor size. Head Neck 27:1049–1055
Evans HL (1987) Encapsulated papillary neoplasms of the thyroid. A study of 14 cases followed for a minimum of 10 years. Am J Surg Pathol 11:592–597
Ghossein R (2009) Problems and controversies in the histopathology of thyroid carcinomas of follicular cell origin. Arch Pathol Lab Med 133:683–691
Ghossein R (2010) Encapsulated malignant follicular cell-derived thyroid tumors. Endocr Pathol 21:212–218
Hunt J (2005) Understanding the genotype of follicular thyroid tumors. Endocr Pathol 16:311–321
Liu J, Singh B, Tallini G, Carlson DL, Katabi N, Shaha A, Tuttle RM, Ghossein RA (2006) Follicular variant of papillary thyroid carcinoma: a clinicopathologic study of a problematic entity. Cancer 107:1255–1264
LiVolsi VA (1990) Surgical pathology of the thyroid. Major problems in pathology, vol 22. W.B. Saunders, Philadelphia
LiVolsi VA, Baloch ZW (2011) Follicular-patterned tumors of the thyroid: the battle of benign vs. malignant vs. so-called uncertain. Endocr Pathol 22:184–189
Lloyd RV, Buehler D, Khanafshar E (2011) Papillary thyroid carcinoma variants. Head Neck Pathol 5:51–56
Máximo V, Sobrinho-Simões M (2000) Hürthle cell tumours of the thyroid. A review with emphasis on mitochondrial abnormalities with clinical relevance. Virchows Arch 437:107–115
Mete O, Asa SL (2011) Pathological definition and clinical significance of vascular invasion in thyroid carcinomas of follicular epithelial derivation. Mod Pathol 24:1545–1552
Moreno A, Rodriguez JM, Sola J, Soria T, Parrilla P (1996) Encapsulated papillary neoplasm of the thyroid: retrospective clinicopathological study with long term follow up. Eur J Surg 162:177–180
Murray D (1998) The thyroid gland. In: Kovacs K, Asa SL (eds) Functional endocrine pathology, 2nd edn. Blackwell Science, Malden, pp 295–380
Musholt TJ, Clerici T, Dralle H, Frilling A, Goretzki PE, Hermann MM, Kussmann J, Lorenz K, Nies C, Schabram J, Schabram P, Scheuba C, Simon D, Steinmüller T, Trupka AW, Wahl RA, Zielke A, Bockisch A, Karges W, Luster M, Schmid KW, Interdisciplinary Task Force Guidelines of the German Association of Endocrine Surgeons (2011) German Association of Endocrine Surgeons practice guidelines for the surgical treatment of benign thyroid disease. Langenbecks Arch Surg 396:639–649
Rivera M, Ricarte-Filho J, Knauf J, Shaha A, Tuttle M, Fagin JA, Ghossein RA (2010) Molecular genotyping of papillary thyroid carcinoma follicular variant according to its histological subtypes (encapsulated vs infiltrative) reveals distinct BRAF and RAS mutation patterns. Mod Pathol 23:1191–1200
Rosai J (2004) Poorly differentiated thyroid carcinoma: introduction to the issue, its landmarks, and clinical impact. Endocr Pathol 15:293–296
Sahoo S, Hoda SA, Rosai J, DeLellis RA (2001) Cytokeratin 19 immunoreactivity in the diagnosis of papillary thyroid carcinoma: a note of caution. Am J Clin Pathol 116:696–702
Salajegheh A, Petcu EB, Smith RA, Lam AK (2008) Follicular variant of papillary thyroid carcinoma: a diagnostic challenge for clinicians and pathologists. Postgrad Med J 84:78–82
Sakamoto A, Kasai N, Sugano H (1983) Poorly differentiated carcinoma of the thyroid. A clinicopathologic entity for a highrisk group of papillary and follicular carcinomas. Cancer 52:1849–1855
Schröder S, Böcker W, Dralle H, Kortmann KB, Stern C (1984) The encapsulated papillary carcinoma of the thyroid. A morphologic subtype of the papillary thyroid carcinoma. Cancer 54:90–93
Serra S, Asa SL (2008) Controversies in thyroid pathology: the diagnosis of follicular neoplasms. Endocr Pathol 19:156–165
Sheu SY, Grabellus F, Schwertheim S, Worm K, Broecker-Preuss M, Schmid KW (2010) Differential miRNA expression profiles in variants of papillary thyroid carcinoma and encapsulated follicular thyroid tumours. Br J Cancer 102:376–382
Sneed DC (1999) Protocol for the examination of specimens from patients with malignant tumors of the thyroid gland, exclusive of lymphomas. Arch Pathol Lab Med 123:45–49
Sobrinho-Simões M, Preto A, Rocha AS, Castro P, Máximo V, Fonseca E, Soares P (2005) Molecular pathology of well-differentiated thyroid carcinomas. Virchows Arch 447:787–793
Sobrinho-Simões M, Máximo V, Rocha AS, Trovisco V, Castro P, Preto A, Lima J, Soares P (2008) Intragenic mutations in thyroid cancer. Endocrinol Metab Clin North Am 37:333–362
Sobrinho-Simões M, Eloy C, Magalhães J, Lobo C, Amaro T (2011) Follicular thyroid carcinoma. Mod Pathol 24(Suppl 2):S10–S18
Trovisco V, Vieira de Castro I, Soares P, Máximo V, Silva P, Magalhães J, Abrosimov A, Guiu XM, Sobrinho-Simões M (2004) BRAF mutations are associated with some histological types of papillary thyroid carcinoma. J Pathol 202:247–251
Volante M, Collini P, Nikiforov YE, Sakamoto A, Kakudo K, Katoh R, Lloyd RV, LiVolsi VA, Papotti M, Sobrinho-Simoes M, Bussolati G, Rosai J (2007) Poorly differentiated thyroid carcinoma: the Turin proposal for the use of uniform diagnostic criteria and an algorithmic diagnostic approach. Am J Surg Pathol 31:1256–1264
Wreesmann VB, Ghossein RA, Hezel M, Banerjee D, Shaha AR, Tuttle RM, Shah JP, Rao PH, Singh B (2004) Follicular variant of papillary thyroid carcinoma: genome-wide appraisal of a controversial entity. Genes Chromosomes Cancer 40:355–364
Wynford-Thomas D (1994) Thyroid cancer. In: Lemoine N, Neoptolemos J, Cooke T (eds) Cancer. A molecular approach. Blackwell Scientific, Oxford, pp 192–222
Xing M (2005) BRAF mutation in thyroid cancer. Endocr Relat Cancer 12:245–262
Zhu Z, Gandhi M, Nikiforova MN, Fischer AH, Nikiforov YE (2003) Molecular profile and clinical–pathologic features of the follicular variant of papillary thyroid carcinoma. An unusually high prevalence of ras mutations. Am J Clin Pathol 120:71–77
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This paper was partly presented and discussed at the workshop “Surgery of Thyroid Cancer” organized by the European Society of Endocrine Surgeons (Berlin, Germany, May 23–25, 2013).
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Dionigi, G., Kraimps, JL., Schmid, K.W. et al. Minimally invasive follicular thyroid cancer (MIFTC)—a consensus report of the European Society of Endocrine Surgeons (ESES). Langenbecks Arch Surg 399, 165–184 (2014). https://doi.org/10.1007/s00423-013-1140-z
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DOI: https://doi.org/10.1007/s00423-013-1140-z
Keywords
- Follicular thyroid carcinoma
- Minimally invasive follicular thyroid carcinoma
- Widely invasive follicular carcinoma
- Histopathology
- Classification
- Vascular invasion
- Capsular invasion
- Surgery
- Diagnosis
- Prognosis
- Adult
- Age
- Tumor size
- Distant metastases
- Recurrence
- Lymph node metastases
- Radio iodine ablation
- Lymphadenectomy