Medullary thyroid cancer diagnosis: An appraisal

Head and Neck

Volumn 36, Issue 8, 2014, Pages 1216-1223

  Trimboli, Pierpaolo ^a   Giovanella, Luca ^b   Crescenzi, Anna ^a,c   Romanelli, Francesco ^d   Valabrega, Stefano ^e   Spriano, Giuseppe ^f   Cremonini, Nadia ^g   Guglielmi, Rinaldo ^c   Papini, Enrico ^c  

^a Piazza San Bartolomeo All'Isola 21   (Italy)

^b ONCOLOGY INSTITUTE OF SOUTHERN SWITZERLAND   (Switzerland)

^c REGINA APOSTOLORUM HOSPITAL   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^g MAGGIORE HOSPITAL   (Italy)

Author keywords

calcitonin; carcinoma; cytology; rearranged during transfection (RET); thyroid

Indexed keywords

CALCITONIN; TUMOR MARKER;

ARTICLE; ASPIRATION CYTOLOGY; BLOOD SAMPLING; CALCITONIN BLOOD LEVEL; CANCER DIAGNOSIS; CLINICAL PRACTICE; COMPUTER ASSISTED TOMOGRAPHY; DIAGNOSTIC ACCURACY; ECHOGRAPHY; FINE NEEDLE ASPIRATION BIOPSY; GENETIC TRANSFECTION; HUMAN; MUTATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; THYROID MEDULLARY CARCINOMA; PATHOLOGY; PROCEDURES; THYROID GLAND; THYROID NEOPLASMS;

BIOPSY, FINE-NEEDLE; HUMANS; MUTATION; THYROID GLAND; THYROID NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 84904253815     PISSN: 10433074     EISSN: 10970347     Source Type: Journal    
DOI: 10.1002/hed.23449     Document Type: Article

References (98)

1. Tuttle M., Medullary thyroid cancer: clinical manifestations, diagnosis and staging. Available at: www.uptodate.com. Accessed August 23, 2013.
2. American Thyroid Association Guidelines Task Force, Kloos RT, Eng C, et al. Medullary thyroid cancer: management guidelines of the American Thyroid Association. Thyroid 2009; 19: 565-612.
3. Kebebew E, Ituarte PH, Siperstein AE, Duh QY, Clark OH,. Medullary thyroid carcinoma: clinical characteristics, treatment, prognostic factors, and a comparison of staging systems. Cancer 2000; 88: 1139-1148.
4. Williams GA, Hargis GK, Galloway WB, Henderson WJ,. Evidence for thyrocalcitonin in man. Proc Soc Exp Biol Med 1966; 122: 1273-1276.
5. Horn RC, Ravdin IS,. Carcinoma of the thyroid gland in youth. J Clin Endocrinol Metab 1951; 11: 1166-1178.
6. Elisei R, Bottici V, Luchetti F, et al. Impact of routine measurement of serum calcitonin on the diagnosis and outcome of medullary thyroid cancer: experience in 10,864 patients with nodular thyroid disorders. J Clin Endocrinol Metab 2004; 89: 163-168.
7. Bugalho MJ, Santos JR, Sobrinho L,. Preoperative diagnosis of medullary thyroid carcinoma: fine needle aspiration cytology as compared with serum calcitonin measurement. J Surg Oncol 2005; 91: 56-60.
8. Costante G, Meringolo D, Durante C, et al. Predictive value of serum calcitonin levels for preoperative diagnosis of medullary thyroid carcinoma in a cohort of 5817 consecutive patients with thyroid nodules. J Clin Endocrinol Metab 2007; 92: 450-455.
9. Cheung K, Roman SA, Wang TS, Walker HD, Sosa JA,. Calcitonin measurement in the evaluation of thyroid nodules in the United States: a cost-effectiveness and decision analysis. J Clin Endocrinol Metab 2008; 93: 2173-2180.
10. Pacini F, Castagna MG, Cipri C, Schlumberger M,. Medullary thyroid carcinoma. Clin Oncol (R Coll Radiol) 2010; 22: 475-485.
11. Tuttle RM, Ball DW, Byrd D, et al. Medullary carcinoma. J Natl Compr Canc Netw 2010; 8: 512-530.
12. Saller B, Görges R, Reinhardt W, Haupt K, Janssen OE, Mann K,. Sensitive calcitonin measurement by two-site immunometric assays: implications for calcitonin screening in nodular thyroid disease. Clin Lab 2002; 48: 191-200.
13. Leboeuf R, Langlois MF, Martin M, Ahnadi CE, Fink GD,. " Hook effect" in calcitonin immunoradiometric assay in patients with metastatic medullary thyroid carcinoma: case report and review of the literature. J Clin Endocrinol Metab 2006; 91: 361-364.
14. Perdrisot R, Bigorgne JC, Guilloteau D, Jallet P,. Monoclonal immunoradiometric assay of calcitonin improves investigation of familial medullary thyroid carcinoma. Clin Chem 1990; 36: 381-383.
15. Zink A, Blind E, Raue F,. Determination of serum calcitonin by immunometric two-site assays in normal subjects and patients with medullary thyroid carcinoma. Eur J Clin Chem Clin Biochem 1992; 30: 831-835.
16. Grauer R, Raue F, Ziegler R,. Clinical usefulness of a new chemiluminescent two-site immunoassay for human calcitonin. Exp Clin Endocrinol Diabetes 1998; 106: 353-359.
17. Bieglmayer C, Vierhapper H, Dudczak R, Niederle B,. Measurement of calcitonin by immunoassay analyzers. Clin Chem Lab Med 2007; 45: 662-666.
18. Barbot N, Calmettes C, Schuffenecker I, et al. Pentagastrin stimulation test and early diagnosis of medullary thyroid carcinoma using an immunoradiometric assay of calcitonin: comparison with genetic screening in hereditary medullary thyroid carcinoma. J Clin Endocrinol Metab 1994; 78: 114-120.
19. Karges W, Dralle HH, Raue F, et al. Calcitonin measurement to detect medullary thyroid carcinoma in nodular goiter: German evidence-based consensus recommendation. Exp Clin Endocrinol Diabetes 2004; 112: 52-58.
20. d'Herbomez M, Caron P, Bauters C, et al. Reference range of serum calcitonin levels in humans: influence of calcitonin assays, sex, age, and cigarette smoking. Eur J Endocrinol 2007; 157: 749-755.
21. Ramachandran R, Benfield P, Dhillo WS, et al. Need for revision of diagnostic limits for medullary thyroid carcinoma with a new immunochemiluminometric calcitonin assay. Clin Chem 2009; 55: 2225-2226.
22. Guyétant S, Rousselet MC, Durigon M, et al. Sex-related C cell hyperplasia in the normal human thyroid: a quantitative autopsy study. J Clin Endocrinol Metab 1997; 82: 42-47.
23. Giovanella L, Imperiali M, Ferrari A, et al. Thyroid volume influences serum calcitonin levels in a thyroid-healthy population: results of a 3-assay, 519 subjects study. Clin Chem Lab Med 2012; 50: 895-900.
24. Toledo SP, Lourenço DM Jr, Santos MA, Tavares MR, Toledo RA, Correia-Deur JE,. Hypercalcitoninemia is not pathognomonic of medullary thyroid carcinoma. Clinics (Sao Paulo) 2009; 64: 699-706.
25. Castro MR, Gharib H,. Continuing controversies in the management of thyroid nodules. Ann Intern Med 2005; 142: 926-931.
26. Erdogan MF, Gursoy A, Kulaksizoglu M,. Long-term effects of elevated gastrin levels on calcitonin secretion. J Endocrinol Invest 2006; 29: 771-775.
27. Vantyghem MC, Danel T, Marcelli-Tourvielle S, et al. Calcitonin levels do not decrease with weaning in chronic alcoholism. Thyroid 2007; 17: 213-217.
28. Giovanella L, Suriano S,. Spurious hypercalcitoninemia and heterophilic antibodies in patients with thyroid nodules. Head Neck 2011; 33: 95-97.
29. Gharib H, Papini E, Paschke R, et al. American Association of Clinical Endocrinologists, Associazione Medici Endocrinologi, and European Thyroid Association medical guidelines for clinical practice for the diagnosis and management of thyroid nodules: executive summary of recommendations. J Endocrinol Invest 2010; 33 (5 Suppl): 51-56.
30. Machens A, Hoffmann F, Sekulla C, Dralle H,. Importance of gender-specific calcitonin thresholds in screening for occult sporadic medullary thyroid cancer. Endocr Relat Cancer 2009; 16: 1291-1298.
31. Ahmed SR, Ball DW,. Clinical review: Incidentally discovered medullary thyroid cancer: diagnostic strategies and treatment. J Clin Endocrinol Metab 2011; 96: 1237-1245.
32. Dora JM, Canalli MH, Capp C, Puñales MK, Vieira JG, Maia AL,. Normal perioperative serum calcitonin levels in patients with advanced medullary thyroid carcinoma: case report and review of the literature. Thyroid 2008; 18: 895-899.
33. Giovanella L, Crippa S, Ceriani L,. Serum calcitonin-negative medullary thyroid carcinoma: role of CgA and CEA as complementary markers. Int J Biol Markers 2008; 23: 129-131.
34. Schlumberger M, Bastholt L, Dralle H, Jarzab B, Pacini F, Smit JWA,. 2012 European Thyroid Association guidelines for metastatic medullary thyroid cancer. Eur Thyroid J 2012; 1: 5-14.
35. Karges W, Dralle H, Raue F, et al. Calcitonin measurement to detect medullary thyroid carcinoma in nodular goiter: German evidence-based consensus recommendation. Exp Clin Endocrinol Diabetes 2004; 112: 52-58.
36. Wells SA Jr, Baylin SB, Linehan WM, Farrell RE, Cox EB, Cooper CW,. Provocative agents and the diagnosis of medullary carcinoma of the thyroid gland. Ann Surg 1978; 188: 139-141.
37. Costante G, Durante C, Francis Z, Schlumberger M, Filetti S,. Determination of calcitonin in C-cell disease: clinical interest and potential pitfalls. Nat Clin Pract Endocrinol Metab 2009; 5: 35-44.
38. Wenig BM, Heffness CS, Adair CF,. Atlas of endocrine pathology. Philadelphia, PA: WB Saunders Company; 1997. p 374.
39. Vierhapper H, Niederle B, Bieglmayer C, Kaserer K, Baumgartner-Parzer S,. Early diagnosis and curative therapy of medullary thyroid carcinoma by routine measurement of serum calcitonin in patients with thyroid disorders. Thyroid 2005; 15: 1267-1272.
40. Doyle P, Düren C, Nerlich K, et al. Potency and tolerance of calcitonin stimulation with high-dose calcium versus pentagastrin in normal adults. J Clin Endocrinol Metab 2009; 94: 2970-2974.
41. Giovanella L,. Serum procalcitonin and calcitonin normal values before and after calcium gluconate infusion. Exp Clin Endocrinol Diabetes 2012; 120: 169-170.
42. Colombo C, Verga U, Mian C, et al. Comparison of calcium and pentagastrin tests for the diagnosis and follow-up of medullary thyroid carcinoma. J Clin Endocrinol Metab 2012; 97: 905-913.
43. Scheuba C, Kaserer K, Bieglmayer C, et al. Medullary thyroid microcarcinoma recommendations for treatment-a single-center experience. Surgery 2007; 142: 1003-1010; discussion 1010.
44. Emmertsen KK, Nielsen HE, Mosekilde L, Hansen HH,. Pentagastrin, calcium and whisky stimulated serum calcitonin in medullary carcinoma of the thyroid. Acta Radiol Oncol 1980; 19: 85-89.
45. Vitale G, Ciccarelli A, Caraglia M, et al. Comparison of two provocative tests for calcitonin in medullary thyroid carcinoma: omeprazole vs pentagastrin. Clin Chem 2002; 48: 1505-1510.
46. Machens A, Ukkat J, Hauptmann S, Dralle H,. Abnormal carcinoembryonic antigen levels and medullary thyroid cancer progression: a multivariate analysis. Arch Surg 2007; 142: 289-293; discussion 294.
47. Algeciras-Schimnich A, Preissner CM, Theobald JP, Finseth MS, Grebe SK,. Procalcitonin: a marker for the diagnosis and follow-up of patients with medullary thyroid carcinoma. J Clin Endocrinol Metab 2009; 94: 861-868.
48. Giovanella L, Maffioli M, Suriano S, Dorizzi RM,. Elevated calcitonin and procalcitonin levels in nonmedullary benign and malignant thyroid nodules. Clin Endocrinol (Oxf) 2010; 72: 852-853.
49. Kratzsch J, Petzold A, Raue F, at al. Basal and stimulated calcitonin and procalcitonin in various assays in patients with and without medullary thyroid cancer. Clin Chem 2011; 57: 467-474.
50. Giovanella L, Verburg FA, Imperiali M, Valabrega S, Trimboli P, Ceriani L,. Comparison of serum calcitonin and procalcitonin in detecting medullary thyroid carcinoma among patients with thyroid nodules. Clin Chem Lab Med 2013; 51: 1477-1481.
51. Rago T, Vitti P, Chiovato L, et al. Role of conventional ultrasonography and color flow-Doppler sonography in predicting malignancy in 'cold' thyroid nodules. Eur J Endocrinol 1998; 138: 41-46.
52. Papini E, Guglielmi R, Bianchini A, et al. Risk of malignancy in nonpalpable thyroid nodules: predictive value of ultrasound and color-Doppler features. J Clin Endocrinol Metab 2002; 87: 1941-1946.
53. Gorman B, Charboneau JW, James EM, et al. Medullary thyroid carcinoma: role of high-resolution US. Radiology 1987; 162(1 Pt 1): 147-150.
54. Saller B, Moeller L, Görges R, Janssen OE, Mann K,. Role of conventional ultrasound and color Doppler sonography in the diagnosis of medullary thyroid carcinoma. Exp Clin Endocrinol Diabetes 2002; 110: 403-407.
55. Kim SH, Kim BS, Jung SL, et al. Ultrasonographic findings of medullary thyroid carcinoma: a comparison with papillary thyroid carcinoma. Korean J Radiol 2009; 10: 101-105.
56. Lee S, Shin JH, Han BK, Ko EY,. Medullary thyroid carcinoma: comparison with papillary thyroid carcinoma and application of current sonographic criteria. AJR Am J Roentgenol 2010; 194: 1090-1094.
57. Choi N, Moon WJ, Lee JH, Baek JH, Kim DW, Park SW,. Ultrasonographic findings of medullary thyroid cancer: differences according to tumor size and correlation with fine needle aspiration results. Acta Radiol 2011; 52: 312-316.
58. Trimboli P, Nasrollah N, Amendola S, et al. Should we use ultrasound features associated with papillary thyroid cancer in diagnosing medullary thyroid cancer? Endocr J 2012; 59: 503-508.
59. Fukushima M, Ito Y, Hirokawa M, et al. Excellent prognosis of patients with nonhereditary medullary thyroid carcinoma with ultrasonographic findings of follicular tumor or benign nodule. World J Surg 2009; 33: 963-968.
60. Seo YL, Yoon DY, Baek S, et al. Detection of neck recurrence in patients with differentiated thyroid cancer: comparison of ultrasound, contrast-enhanced CT and (18)F-FDG PET/CT using surgical pathology as a reference standard: (ultrasound vs. CT vs. (18)F-FDG PET/CT in recurrent thyroid cancer). Eur Radiol 2012; 22: 2246-2254.
61. Kauhanen S, Schalin-Jäntti C, Seppänen M, et al. Complementary roles of 18F-DOPA PET/CT and 18F-FDG PET/CT in medullary thyroid cancer. J Nucl Med 2011; 52: 1855-1863.
62. Kini SR,. Thyroid Cytopathology. An atlas and text. Philadelphia, PA: Lippincott Williams & Wilkins; 2008. p 550.
63. DeLellis RA, Lloyd RV, Heitz PU, Eng C., WHO Classification of Tumours. Pathology and Genetics of Tumours of Endocrine Organs. Lyon, France: IARC Press; 2004.
64. Bhanot P, Yang J, Schnadig VJ, Logroño R,. Role of FNA cytology and immunochemistry in the diagnosis and management of medullary thyroid carcinoma: report of six cases and review of the literature. Diagn Cytopathol 2007; 35: 285-292.
65. Ross DS,. Atlas of Thyroid Cytopathology. UptoDate. Available at: www.uptodate.com. Accessed August 23, 2013.
66. De May RM,. The art and science of cytopathology, aspiration cytology. Chicago, IL: ASCP Press; 1996. p 703.
67. Park KT, Ahn SH, Mo JH, et al. Role of core needle biopsy and ultrasonographic finding in management of indeterminate thyroid nodules. Head Neck 2011; 33: 160-165.
68. Papaparaskeva K, Nagel H, Droese M,. Cytologic diagnosis of medullary carcinoma of the thyroid gland. Diagn Cytopathol 2000; 22: 351-358.
69. Forrest CH, Frost FA, de Boer WB, Spagnolo DV, Whitaker D, Sterrett BF,. Medullary carcinoma of the thyroid: accuracy of diagnosis of fine-needle aspiration cytology. Cancer 1988; 84: 295-302.
70. Dustin SM, Jo VY, Hanley KZ, Stelow EB,. High sensitivity and positive predictive value of fine-needle aspiration for uncommon thyroid malignancies. Diagn Cytopathol 2012; 40: 416-421.
71. Boi F, Maurelli I, Pinna G, et al. Calcitonin measurement in wash-out fluid from fine needle aspiration of neck masses in patients with primary and metastatic medullary thyroid carcinoma. J Clin Endocrinol Metab 2007; 92: 2115-2118.
72. Kudo T, Miyauchi A, Ito Y, Takamura Y, Amino N, Hirokawa M,. Diagnosis of medullary thyroid carcinoma by calcitonin measurement in fine-needle aspiration biopsy specimens. Thyroid 2007; 17: 635-638.
73. Massaro F, Dolcino M, Degrandi R, et al. Calcitonin assay in wash-out fluid after fine-needle aspiration biopsy in patients with a thyroid nodule and border-line value of the hormone. J Endocrinol Invest 2009; 32: 308-312.
74. Abraham D, Gault PM, Hunt J, Bentz J,. Calcitonin estimation in neck lymph node fine-needle aspirate fluid prevents misinterpretation of cytology in patients with metastatic medullary thyroid cancer. Thyroid 2009; 19: 1015-1016.
75. Trimboli P, Rossi F, Baldelli R, et al. Measuring calcitonin in washout of the needle in patients undergoing fine needle aspiration with suspicious medullary thyroid cancer. Diagn Cytopathol 2012; 40: 394-398.
76. Trimboli P, Nigri G, Romanelli F, et al. Medullary thyroid nodules by measurement of calcitonin (Ct) in aspiration needle washout in patients with multinodular goiter and moderately elevated serum Ct. Exp Clin Endocrinol Diabetes 2012; 120: 234-237.
77. Giovanella L, Ceriani L, Bongiovanni M,. Calcitonin measurement on fine needle washouts: preanalytical issues and normal reference values. Diagn Cytopathol 2013; 41: 226-229.
78. Eng C, Mulligan LM, Smith DP, et al. Low frequency of germline mutations in the RET proto-oncogene in patients with apparently sporadic medullary thyroid carcinoma. Clin Endocrinol (Oxf) 1995; 43: 123-127.
79. Wohllk N, Cote GJ, Bugalho MM, et al. Relevance of RET proto-oncogene mutations in sporadic medullary thyroid carcinoma. J Clin Endocrinol Metab 1996; 81: 3740-3745.
80. Schuffenecker I, Ginet N, Goldgar D, et al. Prevalence and parental origin of de novo RET mutations in multiple endocrine neoplasia type 2A and familial medullary thyroid carcinoma. Le Groupe d'Etude des Tumeurs a Calcitonine. Am J Hum Genet 1997; 60: 233-237.
81. Romei C, Cosci B, Renzini G, et al. RET genetic screening of sporadic medullary thyroid cancer (MTC) allows the preclinical diagnosis of unsuspected gene carriers and the identification of a relevant percentage of hidden familial MTC (FMTC). Clin Endocrinol (Oxf) 2011; 74: 241-247.
82. Mulligan LM, Kwok JB, Healey CS, et al. Germ-line mutations of the RET proto-oncogene in multiple endocrine neoplasia type 2A. Nature 1993; 363: 458-460.
83. Donis-Keller H, Dou S, Chi D, et al. Mutations in the RET proto-oncogene are associated with MEN 2A and FMTC. Hum Mol Genet 1993; 2: 851-856.
84. Eng C, Smith DP, Mulligan LM, et al. Point mutation within the tyrosine kinase domain of the RET proto-oncogene in multiple endocrine neoplasia type 2B and related sporadic tumours. Hum Mol Genet 1994; 3: 237-241.
85. Eng C, Clayton D, Schuffenecker I, et al. The relationship between specific RET proto-oncogene mutations and disease phenotype in multiple endocrine neoplasia type 2. International RET mutations consortium analysis. JAMA 1996; 276: 1575-1579.
86. Moline J, Eng C,. Multiple endocrine neoplasia type 2: an overview. Genet Med 2011; 13: 755-764.
87. Mulligan LM, Eng C, Attié T, et al. Diverse phenotypes associated with exon 10 mutations of the RET proto-oncogene. Hum Mol Genet 1994; 3: 2163-2167.
88. Machens A, Niccoli-Sire P, Hoegel J, et al. Early malignant progression of hereditary medullary thyroid cancer. N Engl J Med 2003; 349: 1517-1525.
89. Brandi ML, Gagel RF, Angeli A, et al. Guidelines for diagnosis and therapy of MEN type I and type 2. J Clin Endocrinol Metab 2001; 86: 5658-5671.
90. Rohmer V, Vidal-Trecan G, Bourdelot A, et al. Prognostic factors of disease-free survival after thyroidectomy in 170 young patients with a RET germline mutation: a multicenter study of the Groupe Franais d'Etude des Tumeurs Endocrines. J Clin Endocrinol Metab 2011; 96: E509-E518.
91. Elisei R, Romei C, Renzini G, et al. The timing of total thyroidectomy in RET gene mutation carriers could be personalized and safely planned on the basis of serum calcitonin: 18 years experience at one single center. J Clin Endocrinol Metab 2012; 97: 426-435.
92. Hofstra RM, Landsvater RM, Ceccherini I, et al. A mutation in the RET proto-oncogene associated with multiple endocrine neoplasia type 2B and sporadic medullary thyroid carcinoma. Nature 1994; 367: 375-376.
93. Marsh DJ, Learoyd DL, Andrew SD, et al. Somatic mutations in the RET proto-oncogene in sporadic medullary thyroid carcinoma. Clin Endocrinol (Oxf) 1996; 44: 249-257.
94. Romei C, Elisei R, Pinchera A, et al. Somatic mutations of the ret protooncogene in sporadic medullary thyroid carcinoma are not restricted to exon 16 and are associated with tumor recurrence. J Clin Endocrinol Metab 1996; 81: 1619-1622.
95. de Groot JW, Links TP, Plukker JT, Lips CJ, Hofstra RM,. RET as a diagnostic and therapeutic target in sporadic and hereditary endocrine tumors. Endocr Rev 2006; 27: 535-560.
96. Elisei R, Cosci B, Romei C, et al. Prognostic significance of somatic RET oncogene mutations in sporadic medullary thyroid cancer: a 10-year follow-up study. J Clin Endocrinol Metab 2008; 93: 682-687.
97. Zedenius J, Larsson C, Bergholm U, et al. Mutations of codon 918 in the RET proto-oncogene correlate to poor prognosis in sporadic medullary thyroid carcinoma. J Clin Endocrinol Metab 1995; 80: 3088-3090.
98. Schilling T, Bürck J, Sinn HP, et al. Prognostic value of codon 918 (ATG->ACG) RET proto-oncogene mutations in sporadic medullary thyroid carcinoma. Int J Cancer 2001; 95: 62-66.