Skip to main content
Top
Published in: Virchows Archiv 3/2008

01-03-2008 | Original Article

A score based on microscopic criteria proposed for analysis of papillary carcinoma of the thyroid

Authors: Priscilla Verhulst, Patrick Devos, Sébastien Aubert, David Buob, Isaac Cranshaw, Christine Do Cao, François Pattou, Bruno Carnaille, Jean-Louis Wemeau, Emmanuelle Leteurtre

Published in: Virchows Archiv | Issue 3/2008

Login to get access

Abstract

Morphologic examination is the gold standard for diagnosing papillary thyroid carcinoma (PTC). This diagnosis, especially for the follicular variant, may be variable even among experts. Our objective was to analyze the frequency of PTC microscopic criteria in a series of thyroid tumors including follicular adenoma (FA) and PTC to build a score which could constitute a novel way for microscopic analysis of such thyroid tumors. Sixty-six PTC and 66 FA were matched for age, sex, and thyroiditis. Two independent observers delineated the classical PTC microscopic criteria. PTC microscopic criteria were variably expressed in individual tumors. Under univariate analysis, all criteria were significantly more frequent in PTC than in FA (p < 0.05). Under multivariate analysis, the most important criteria were: dark staining colloid >25%, nuclear grooves, enlarged nuclei, ovoid nuclei >5% of tumor cells, and lack of polarization. Using linear discriminant analysis, these five criteria allowed us to build a scaled score. The score proposed did not allow the making of a definite distinction between FA and PTC in routine practice. It represents the variety of microscopic presentations of FA and PTC on the basis of a statistical analysis and could help in further evaluation of immunohistochemical or molecular markers.
Literature
1.
go back to reference Adeniran AJ, Zhu Z, Gandhi M, Steward DL, Fidler JP, Giordano TJ, Biddinger PW, Nikiforov Y (2006) Correlation between genetic alterations and microscopic features, clinical manifestations and prognostic characteristics of thyroid papillary carcinomas. Am J Surg Pathol 30:216–222PubMedCrossRef Adeniran AJ, Zhu Z, Gandhi M, Steward DL, Fidler JP, Giordano TJ, Biddinger PW, Nikiforov Y (2006) Correlation between genetic alterations and microscopic features, clinical manifestations and prognostic characteristics of thyroid papillary carcinomas. Am J Surg Pathol 30:216–222PubMedCrossRef
2.
go back to reference Baloch ZW, Livolsi VA (2002) Follicular-patterned lesions of the thyroid: the bane of the pathologist. Am J Clin Pathol 117:143–150PubMedCrossRef Baloch ZW, Livolsi VA (2002) Follicular-patterned lesions of the thyroid: the bane of the pathologist. Am J Clin Pathol 117:143–150PubMedCrossRef
3.
go back to reference Baloch ZW, LiVolsi VA (2005) Pathologic diagnosis of papillary thyroid carcinoma: today and tomorrow. Expert Rev Mol Diagn 5:573–584PubMedCrossRef Baloch ZW, LiVolsi VA (2005) Pathologic diagnosis of papillary thyroid carcinoma: today and tomorrow. Expert Rev Mol Diagn 5:573–584PubMedCrossRef
4.
go back to reference Baloch ZW, LiVolsi VA (2007) Our approach to follicular-patterned lesions of the thyroid. J Clin Pathol 60:244–250PubMedCrossRef Baloch ZW, LiVolsi VA (2007) Our approach to follicular-patterned lesions of the thyroid. J Clin Pathol 60:244–250PubMedCrossRef
5.
go back to reference Barroeta JE, Baloch ZW, Lal P, Pasha TL, Zhang PJ, LiVolsi VA (2006) Diagnostic value of differential expression of CK19, Galectin-3, HBME-1, ERK, RET, and p16 in benign and malignant follicular-derived lesions of the thyroid: an immunohistochemical tissue microarray analysis. Endocr Pathol 17:225–234PubMedCrossRef Barroeta JE, Baloch ZW, Lal P, Pasha TL, Zhang PJ, LiVolsi VA (2006) Diagnostic value of differential expression of CK19, Galectin-3, HBME-1, ERK, RET, and p16 in benign and malignant follicular-derived lesions of the thyroid: an immunohistochemical tissue microarray analysis. Endocr Pathol 17:225–234PubMedCrossRef
6.
go back to reference Castro P, Rebocho AP, Soares RJ, Magalhaes J, Roque L, Trovisco V, Vieira de Castro I, Cardoso-de-Oliveira M, Fonseca E, Soares P, Sobrinho-Simoes M (2006) PAX8-PPARgamma rearrangement is frequently detected in the follicular variant of papillary thyroid carcinoma. J Clin Endocrinol Metab 91:213–220PubMedCrossRef Castro P, Rebocho AP, Soares RJ, Magalhaes J, Roque L, Trovisco V, Vieira de Castro I, Cardoso-de-Oliveira M, Fonseca E, Soares P, Sobrinho-Simoes M (2006) PAX8-PPARgamma rearrangement is frequently detected in the follicular variant of papillary thyroid carcinoma. J Clin Endocrinol Metab 91:213–220PubMedCrossRef
7.
go back to reference Chan JK (2002) Strict criteria should be applied in the diagnosis of encapsulated follicular variant of papillary thyroid carcinoma. Am J Clin Pathol 117:16–18PubMedCrossRef Chan JK (2002) Strict criteria should be applied in the diagnosis of encapsulated follicular variant of papillary thyroid carcinoma. Am J Clin Pathol 117:16–18PubMedCrossRef
8.
go back to reference Chan JKC (2002) The author's reply. Am J Clin Pathol 118:605 Chan JKC (2002) The author's reply. Am J Clin Pathol 118:605
9.
go back to reference Chevillard S, Ugolin N, Vielh P, Ory K, Levalois C, Elliott D, Clayman GL, El-Naggar AK (2004) Gene expression profiling of differentiated thyroid neoplasms: diagnostic and clinical implications. Clin Cancer Res 10:6586–6597PubMedCrossRef Chevillard S, Ugolin N, Vielh P, Ory K, Levalois C, Elliott D, Clayman GL, El-Naggar AK (2004) Gene expression profiling of differentiated thyroid neoplasms: diagnostic and clinical implications. Clin Cancer Res 10:6586–6597PubMedCrossRef
10.
go back to reference Ciampi R, Nikiforov YE (2007) Minireview: RET/PTC rearrangements and BRAF mutations in thyroid tumorigenesis. Endocrinology 148:936–941PubMedCrossRef Ciampi R, Nikiforov YE (2007) Minireview: RET/PTC rearrangements and BRAF mutations in thyroid tumorigenesis. Endocrinology 148:936–941PubMedCrossRef
11.
go back to reference Cohen Y, Xing M, Mambo E, Guo Z, Wu G, Trink B, Beller U, Westra WH, Ladenson PW, Sidransky D (2003) BRAF mutation in papillary thyroid carcinoma. J Natl Cancer Inst 95:625–627PubMedCrossRef Cohen Y, Xing M, Mambo E, Guo Z, Wu G, Trink B, Beller U, Westra WH, Ladenson PW, Sidransky D (2003) BRAF mutation in papillary thyroid carcinoma. J Natl Cancer Inst 95:625–627PubMedCrossRef
12.
go back to reference Davies L, Welch HG (2006) Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA 295:2164–2167PubMedCrossRef Davies L, Welch HG (2006) Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA 295:2164–2167PubMedCrossRef
13.
go back to reference De Matos PS, Ferreira AP, De Oliveira Facuri F, Assumpçao LVM, Metze K, Ward LS (2005) Usefulness of HBME-1, cytokeratin 19 and galectin-3 immunostaining in the diagnosis of thyroid malignancy. Histopathology 47:391–401PubMedCrossRef De Matos PS, Ferreira AP, De Oliveira Facuri F, Assumpçao LVM, Metze K, Ward LS (2005) Usefulness of HBME-1, cytokeratin 19 and galectin-3 immunostaining in the diagnosis of thyroid malignancy. Histopathology 47:391–401PubMedCrossRef
14.
go back to reference Di Cristofaro J, Marcy M, Vasko V, Sebag F, Fakhry N, Wynford-Thomas D, De Micco C (2006) Molecular genetic study comparing follicular variant versus classic papillary thyroid carcinomas: association of N-ras mutation in codon 61 with follicular variant. Hum Pathol 37:824–830PubMedCrossRef Di Cristofaro J, Marcy M, Vasko V, Sebag F, Fakhry N, Wynford-Thomas D, De Micco C (2006) Molecular genetic study comparing follicular variant versus classic papillary thyroid carcinomas: association of N-ras mutation in codon 61 with follicular variant. Hum Pathol 37:824–830PubMedCrossRef
15.
go back to reference Finley DJ, Arora N, Zhu B, Gallagher L, Fahey III TJ (2004) Molecular profiling distinguishes papillary carcinoma from benign thyroid nodules. J Clin Endocrinol Metab 89:3214–3223PubMedCrossRef Finley DJ, Arora N, Zhu B, Gallagher L, Fahey III TJ (2004) Molecular profiling distinguishes papillary carcinoma from benign thyroid nodules. J Clin Endocrinol Metab 89:3214–3223PubMedCrossRef
16.
go back to reference Finley DJ, Zhu B, Barden CB, Fahey TJ (2004) Discrimination of benign and malignant thyroid nodules by molecular profiling. Ann Surg 240:425–437PubMedCrossRef Finley DJ, Zhu B, Barden CB, Fahey TJ (2004) Discrimination of benign and malignant thyroid nodules by molecular profiling. Ann Surg 240:425–437PubMedCrossRef
17.
go back to reference Finn SP, Smyth P, Cahill S, Streck C, O'Regan EM, Flavin R, Sherlock J, Howells D, Henfrey R, Cullen M, Toner M, Timon C, O'Leary JJ, Sheils OM (2007) Expression microarray analysis of papillary thyroid carcinoma and benign thyroid tissue: emphasis on the follicular variant and potential markers of malignancy. Virchows Arch 450:249–260PubMedCrossRef Finn SP, Smyth P, Cahill S, Streck C, O'Regan EM, Flavin R, Sherlock J, Howells D, Henfrey R, Cullen M, Toner M, Timon C, O'Leary JJ, Sheils OM (2007) Expression microarray analysis of papillary thyroid carcinoma and benign thyroid tissue: emphasis on the follicular variant and potential markers of malignancy. Virchows Arch 450:249–260PubMedCrossRef
18.
go back to reference Franc B (2003) Cherche marqueur désespérément pour tumeurs thyroïdiennes de diagnostic incertain. Ann Pathol 23:7–10PubMed Franc B (2003) Cherche marqueur désespérément pour tumeurs thyroïdiennes de diagnostic incertain. Ann Pathol 23:7–10PubMed
19.
go back to reference 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 26:1508–1514PubMedCrossRef 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 26:1508–1514PubMedCrossRef
20.
go back to reference Hunt JL, Dacic S, Barnes EL, Bures JC (2002) Encapsulated follicular variant of papillary thyroid carcinoma. Am J Clin Pathol 118:602–606PubMed Hunt JL, Dacic S, Barnes EL, Bures JC (2002) Encapsulated follicular variant of papillary thyroid carcinoma. Am J Clin Pathol 118:602–606PubMed
21.
go back to reference Kakudo K, Katoh R, Sakamoto A, Asa S, DeLellis RA, Carney JA, Naganuma H, Kameyama K, Takami H (2002) Thyroid gland: international case conference. Endocr Pathol 13:131–134PubMedCrossRef Kakudo K, Katoh R, Sakamoto A, Asa S, DeLellis RA, Carney JA, Naganuma H, Kameyama K, Takami H (2002) Thyroid gland: international case conference. Endocr Pathol 13:131–134PubMedCrossRef
22.
go back to reference Kim J, Giuliano AE, Turner RR, Gaffney RE, Umetani N, Kitago M, Elashoff D, Hoon DSB (2006) Lymphatic mapping establishes the role of BRAF gene mutation in papillary thyroid carcinoma. Ann Surg 244:799–804PubMedCrossRef Kim J, Giuliano AE, Turner RR, Gaffney RE, Umetani N, Kitago M, Elashoff D, Hoon DSB (2006) Lymphatic mapping establishes the role of BRAF gene mutation in papillary thyroid carcinoma. Ann Surg 244:799–804PubMedCrossRef
23.
go back to reference Kondo T, Ezzat S, Asa S (2006) Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat Rev Cancer 6:292–306PubMedCrossRef Kondo T, Ezzat S, Asa S (2006) Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat Rev Cancer 6:292–306PubMedCrossRef
24.
go back to reference Lang BHH, Lo CY, Chan WF, Lam AKY, Wan KY (2006) Classical and follicular variant of papillary thyroid carcinoma: a comparative study on clinicopathologic features and long-term outcome. World J Surg 30:752–758PubMedCrossRef Lang BHH, Lo CY, Chan WF, Lam AKY, Wan KY (2006) Classical and follicular variant of papillary thyroid carcinoma: a comparative study on clinicopathologic features and long-term outcome. World J Surg 30:752–758PubMedCrossRef
25.
go back to reference LiVolsi VA (2003) Can we agree to disagree? Hum Pathol 34:1081–1082PubMed LiVolsi VA (2003) Can we agree to disagree? Hum Pathol 34:1081–1082PubMed
26.
go back to reference LiVolsi VA, Albores-Saavedra J, Asa SL, Baloch ZW, Sobrinho-Simoes M, Wenig B, DeLellis RA, Cady B, Mazzaferri EL, Hay I, Fagin JA, Weber AL, Caruso P, Voutilainen PE, Franssila KO, Williams ED, Schneider AB, Nikiforov Y, Rabes HM, Akslen L, Ezzat S, Santoro M, Eng C, Harach HR (2004) Papillary carcinoma. In: WHO classification of tumours. Pathology and genetics. Tumours of endocrine organs. IARC, Lyon, pp 57–66 LiVolsi VA, Albores-Saavedra J, Asa SL, Baloch ZW, Sobrinho-Simoes M, Wenig B, DeLellis RA, Cady B, Mazzaferri EL, Hay I, Fagin JA, Weber AL, Caruso P, Voutilainen PE, Franssila KO, Williams ED, Schneider AB, Nikiforov Y, Rabes HM, Akslen L, Ezzat S, Santoro M, Eng C, Harach HR (2004) Papillary carcinoma. In: WHO classification of tumours. Pathology and genetics. Tumours of endocrine organs. IARC, Lyon, pp 57–66
27.
go back to reference Lloyd RV, Erickson LA, Casey MB, Lam KY, Lohse CM, Asa SL, Chan JK, DeLellis RA, Harach HR, Kakudo K, LiVolsi VA, Rosai J, Sebo TJ, Sobrinho-Simoes M, Wenig BM, Lae ME (2004) Observer variation in the diagnosis of follicular variant of papillary thyroid carcinoma. Am J Surg Pathol 28:1336–1340PubMed Lloyd RV, Erickson LA, Casey MB, Lam KY, Lohse CM, Asa SL, Chan JK, DeLellis RA, Harach HR, Kakudo K, LiVolsi VA, Rosai J, Sebo TJ, Sobrinho-Simoes M, Wenig BM, Lae ME (2004) Observer variation in the diagnosis of follicular variant of papillary thyroid carcinoma. Am J Surg Pathol 28:1336–1340PubMed
28.
go back to reference Mehrotra P, Okpokam A, Bouhaidar R, Johnson SJ, Wilson JA, Davies BR, Lennard TWJ (2004) Galectin-3 does not reliably distinguish benign from malignant thyroid neoplasms. Histopathology 45:493–500PubMedCrossRef Mehrotra P, Okpokam A, Bouhaidar R, Johnson SJ, Wilson JA, Davies BR, Lennard TWJ (2004) Galectin-3 does not reliably distinguish benign from malignant thyroid neoplasms. Histopathology 45:493–500PubMedCrossRef
29.
go back to reference Nakamura N, Erickson LA, Jin L, Kajita S, Zhang H, Qian X, Rumilla K, Lloyd RV (2006) Immunohistochemical separation of follicular variant of papillary thyroid carcinoma from follicular adenoma. Endocr Pathol 17:213–223PubMedCrossRef Nakamura N, Erickson LA, Jin L, Kajita S, Zhang H, Qian X, Rumilla K, Lloyd RV (2006) Immunohistochemical separation of follicular variant of papillary thyroid carcinoma from follicular adenoma. Endocr Pathol 17:213–223PubMedCrossRef
30.
go back to reference Papotti M, Manazza AD, Chiarle R, Bussolati G (2004) Confocal microscope analysis and tridimensional reconstruction of papillary thyroid carcinoma nuclei. Virchows Arch 444:350–355PubMedCrossRef Papotti M, Manazza AD, Chiarle R, Bussolati G (2004) Confocal microscope analysis and tridimensional reconstruction of papillary thyroid carcinoma nuclei. Virchows Arch 444:350–355PubMedCrossRef
31.
go back to reference Papotti M, Rodriguez J, De Pompa R, Bartolazzi A, Rosai J (2005) Galectin-3 and HBME-1 expression in well-differentiated thyroid tumors with follicular architecture of uncertain malignant potential. Mod Pathol 18:541–546PubMedCrossRef Papotti M, Rodriguez J, De Pompa R, Bartolazzi A, Rosai J (2005) Galectin-3 and HBME-1 expression in well-differentiated thyroid tumors with follicular architecture of uncertain malignant potential. Mod Pathol 18:541–546PubMedCrossRef
32.
go back to reference Renshaw AA, Gould EW (2002) Why there is the tendency to “overdiagnose” the follicular variant of papillary thyroid carcinoma. Am J Clin Pathol 117:19–21PubMedCrossRef Renshaw AA, Gould EW (2002) Why there is the tendency to “overdiagnose” the follicular variant of papillary thyroid carcinoma. Am J Clin Pathol 117:19–21PubMedCrossRef
33.
go back to reference Rosai J, Carcangiu ML, DeLellis RA (1992) Atlas of tumor pathology. Tumors of the thyroid gland. Armed Forces Institute of Pathology, Washington, DC Rosai J, Carcangiu ML, DeLellis RA (1992) Atlas of tumor pathology. Tumors of the thyroid gland. Armed Forces Institute of Pathology, Washington, DC
34.
go back to reference Rosen J, He M, Umbricht C, Alexander HR, Dackiw APB, Zeiger MA, Libutti SK (2005) A six-gene model for differentiating benign from malignant thyroid tumors on the basis of gene expression. Surgery 138:1050–1057CrossRef Rosen J, He M, Umbricht C, Alexander HR, Dackiw APB, Zeiger MA, Libutti SK (2005) A six-gene model for differentiating benign from malignant thyroid tumors on the basis of gene expression. Surgery 138:1050–1057CrossRef
35.
go back to reference Scognamiglio T, Hyjek E, Kao J, Chen YT (2006) Diagnostic usefulness of HBME1, galectin-3, CK19 and CITED1 and evaluation of their expression in encapsulated lesions with questionable features of papillary thyroid carcinoma. Am J Clin Pathol 126:700–708PubMedCrossRef Scognamiglio T, Hyjek E, Kao J, Chen YT (2006) Diagnostic usefulness of HBME1, galectin-3, CK19 and CITED1 and evaluation of their expression in encapsulated lesions with questionable features of papillary thyroid carcinoma. Am J Clin Pathol 126:700–708PubMedCrossRef
36.
go back to reference Suster S (2006) Thyroid tumors with a follicular growth pattern. Arch Pathol Lab Med 130:984–988PubMed Suster S (2006) Thyroid tumors with a follicular growth pattern. Arch Pathol Lab Med 130:984–988PubMed
37.
go back to reference Williams ED (2000) Guest editorial: two proposals regarding the terminology of thyroid tumors. Int J Surg Pathol 8:181–183PubMedCrossRef Williams ED (2000) Guest editorial: two proposals regarding the terminology of thyroid tumors. Int J Surg Pathol 8:181–183PubMedCrossRef
Metadata
Title
A score based on microscopic criteria proposed for analysis of papillary carcinoma of the thyroid
Authors
Priscilla Verhulst
Patrick Devos
Sébastien Aubert
David Buob
Isaac Cranshaw
Christine Do Cao
François Pattou
Bruno Carnaille
Jean-Louis Wemeau
Emmanuelle Leteurtre
Publication date
01-03-2008
Publisher
Springer-Verlag
Published in
Virchows Archiv / Issue 3/2008
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-008-0577-x

Other articles of this Issue 3/2008

Virchows Archiv 3/2008 Go to the issue