Abstract
The latest World Health Organization International Classification defines papillary thyroid carcinoma by its “follicular cell differentiation ... as well as characteristic nuclear changes”. However the oxyphilic (Hürthle cell) papillary carcinoma have nuclei which generally resemble the nuclei seen in oxyphilic follicular carcinomas, and such oxyphilic papillary tumors may behave more aggressively than typical papillary cancers. To further characterize these rare tumors, we identified during a 32-year period 22 patients with oxyphilic papillary cancer and compared them with 1,084 patients with typical papillary cancers and 57 patients with oxyphilic follicular cancers treated by the Mayo surgical group during the same time period. Although typical papillary and oxyphilic papillary cancers were comparable with regards to patient age, tumor size and extent, TNM stage, and prognostic score (AGES), there were significant differences. Compared to typical papillary tumors, oxyphilic papillary cancers had fewer neck nodal metastases at primary diagnosis (5% vs 40%,p<0.0001), were more often DNA non-diploid (71% vs 21%,p<0.001), and after 10 postoperative years had higher rates of both tumor recurrence (28% vs 11%,p<0.0001) and cause-specific mortality (1.7% vs 4%,p<0.0005). In these four important respects the oxyphilic papillary cancers more resembled the oxyphilic follicular cancers. For oxyphilic follicular cancers, the frequency of initial neck nodal metastases was 7% (cf 5%); 83% of the oxyphilic follicular tumors were non-diploid (cf 71%), and at 10 years postoperatively the tumor recurrence and cause-specific mortality rates were 28% and 18%, insignificantly different from 28% and 17% seen with the oxyphilic papillary cancers. These results demonstrate that oxyphilic papillary tumors are more similar to oxyphilic follicular than typical papillary cancers, and suggest that in a differentiated follicular cell-derived carcinoma a predominance of oxyphilic cells may be a prognostically more relevant feature than the individual tumor's predominant papillary or follicular morphologic pattern. Perhaps in future Histologic Classifications the World Health Organization should group the oxyphilic papillary cancers with the oxyphilic follicular rather than the typical papillary carcinomas.
Résumé
La dernière version de la Classification Internationale de l'OMS définit le cancer papillaire de la thyroïde par rapport à la “différentiation cellulaire folliculaire ... comme des changements nucléaires caractéristiques”. Le cancer papillaire oxyphilique (de cellules de Hürtle) (OP) a des noyaux qui ressemblent aux noyaux généralement vus dans les cancers folliculaires oxyphiliques (OF). Les cancers OP ont une malignité plus élevée que les cancers papillaires typiques. Afin de caractériser ces cancers rares, nous avons identifié 22 patients ayant un cancer OP, observés pendant une période de 32 ans et nous les avons comparés à 1084 patients ayant un cancer TP et à 57 patients ayant un cancer OF traités pendant la même période de temps à la Mayo Clinic. Bien que les cancers TP et OP étaient comparables selon le sexe, la taille et l'étendue tumorales, le stade TMN, et le score AGES, il y avait des différences significatives. Comparées aux tumeurs TP, les cancers OP avaient moins de métastases cervicales (NNM) au moment du diagnostic initial (5% vs 40%,p<0.0001), étaient plus souvent nondiploïdes pour l'ADN (71% vs 21%,p<0.001), et après 10 ans d'évolution, avaient le taux le plus élevé de récidive tumorale (28% vs 11%,p<0.001) et de mortalité spécifique (1.7% vs 4%,p=0.0005). Ainsi, les cancers OP ressemblent beaucoup aux cancers OF. En ce qui concerne les cancers OF, la fréquence de NNM initiale était de 7% (cf 5%); 83% des tumeurs OF étaient du type non-diploïde (cf 71%) et à 10 ans, les taux de récidives tumorales et de mortalité de cause spécifique étaient respectivement de 28% et 18%, très peu différents des taux de 28% et 17% observés avec les cancers OP. Ces résultats démontrent que les tumeurs OP ressemblent plus aux cancers OF, que les cancers TP et suggèrent que dans un cancer folliculaire différencié, la prédominance oxyphilique peut être un facteur pronostique plus important que le caractère papillaire or folliculaire. Peut-être, à l'avenir, les classifications histologiques de l'OMS devrait regrouper les cancers OP avec les cancers OF plutôt qu'avec les cancers TP.
Resumen
La última clasificación internacional de la Organización Mundial de la Salud define el carcinoma papilar de la glándula tiroides en términos de su “diferenciación en células foliculares ... así como sus alteraciones nucleares características”. Sin embargo, el carcinoma papilar oxifílico (PO) (de células de Hürthle) exhibe núcleos celulares similares a los que se observan en los carcinomas foliculares oxifílicos (FO), y tales tumores no pueden comportarse en forma más agresiva que los cánceres papilares típicos (PT). Con el propósito de caracterizar mejor estos raros tumores, identificamos 22 pacientes con cáncer PO en un periodo de 32 años, y los comparamos con 1.084 pacientes con cánceres PT y 57 pacientes con cánceres FO tratados por el grupo quirúrgico de la Clínica Mayo en el mismo periodo. Aunque los pacientes con cánceres PT y FO aparecieron comparables respecto a edad, tamaño y extensión del tumor, estadificación TPN y puntaje AGES, se encontraron diferencias significativas. Comparados con los tumores PT, los cánceres PO exhibieron menos metástasis ganglionares en el cuello en el momento del diagnóstico primario (5% vs 40%,p<0.0001), aparecieron más frecuentemente como DNA no-diploides (71% vs 21%,p<0.001) y luego de 10 años postoperatorios presentaron mayores tasas de recurrencia (28% vs 11%,p<0.0001) y de mortalidad de causa específica (1.7% vs 4%,p=0.0005). En cuanto a estas cuatro características, los cánceres PO se asemejaron más a los cánceres FO. Para los cánceres FO, la frecuencia inicial de metástasis ganglionares en el cuello fue de 7% (CF 5%); 83% de los tumores FO aparecieron no-diploides (cf 71%) y a los 10 años la tasa de recurrencia tumoral y la rata de mortalidad por causa específica fueron 28% y 18%, insignificativamente diferente del 28% y 17% observados en los cánceres PO. Estos resultados demuestran que los tumores PO se asemejan más a los FO que los cánceres PT, y sugieren que en un carcinoma diferenciado derivado de las células foliculares la prevalencia de las células oxifílicas puede representar una característica con mayor valor prognóstico que el patrón morfológico de predominio papilar o folicular. Tal vez las futuras clasificaciones histológicas la OMS deban agrupar los cánceres PO con los FO en vez de hacerlo con los carcinomas PT.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Hedinger, C., Williams, E.D., Sobin, L.H.: Histological typing of thyroid tumors. In International Histological Classification of Tumours, 2nd edition, No. 11., World Health Organization, Berlin-Heidelberg-New York, Springer-Verlag, 1988, pp. 9–11
McConahey, W.M., Hay, I.D., Woolner, L.B., McConahey, W.M., Hay, I.D., Woolner, L.B., van Heerden, J.A., Taylor, W.F.: Papillary thyroid cancer treated at the Mayo Clinic, 1946 through 1970: Initial manifestations, pathologic findings, therapy, and outcome. Mayo Clin. Proc.61:978, 1986
Mazzaferri, E.L.: Papillary thyroid carcinoma: Factors influencing prognosis and current therapy. Semin. Oncol.14:315, 1987
Cohn, K., Bäckdahl, M., Forsslund, G.: Prognostic value of nuclear DNA content in papillary thyroid carcinoma. World J. Surg.8:474, 1984
Hrafnkelsson, J., Stal, O., Enestrom, S., Hrafnkelsson, J., Stal, O., Enestrom, S., Jonasson, J.G., Björnsson, J., Olafsdottir, K., Nordenskjöld, B.: Cellular DNA pattern, S-phase frequency and survival in papillary thyroid cancer. Acta Oncol.27:329, 1988
Hamming, J.F., Schelfhout, L.J.D.M., Cornelisse, C.J., Hamming, J.F., Schelfhout, L.J.D.M., Cornelisse, C.J., van de Velde, C.J.H., Goslings, B.M., Hermans, J., Fleuren, G.J.: Prognostic value of nuclear DNA content in papillary and follicular thyroid cancer. World J. Surg.12:503, 1988
Hay, I.D.: Papillary thyroid carcinoma. Endocrinol. Metab. Clin. North Am.19:545, 1990
Gardner, L.W.: Hürthle-cell tumours of the thyroid. Arch. Pathol.59:372, 1955
Lindsay, S.: Carcinoma of the Thyroid Gland, Springfield, Illinois, Charles C. Thomas, 1960, pp. 30–65
Woolner, L.B., Beahrs, O.H., Black, B.M., Woolner, L.B., Beahrs, O.H., Black, B.M., McConahey, W.M., Keating, F.R.: Classification and prognosis of thyroid carcinoma: A study of 885 cases observed in a thirty-year period. Am. J. Surg.102:354, 1961
Meissner, W.A., Adler, A.: Papillary carcinoma of the thyroid: A study of the pathology of two hundred twenty-six cases. A.M.A. Arch. Pathol.66:518, 1958
Selzer, G., Kahn, L.B., Albertyn, L.: Primary malignant tumours of the thyroid gland: A clinical pathologic study of 254 cases. Cancer40:1501, 1977
Chen, K.T.K.: Fine-needle aspiration cytology of papillary Hürthle-cell tumours of thyroid: A report of three cases. Diagn. Cytopathol.7:53, 1991
Schröder, S., Dralle, H., Rehpenning, W., Schröder, S., Dralle, H., Rehpenning, W., Böcker, W.: Prognosekriterien des papillären Schilddrüsencarcinoms. Morphologisch-Klinische Analyse von 202 Tumour fällen. Langenbecks Arch. Chir.371:263, 1987
Barbuto, D., Carcangiu, M.L., Rosai, J.: Papillary Hürthle cell neoplasms of the thyroid gland: A study of 20 cases (abstract). Lab. Invest.62:7A, 1990
Wu, P.S-C., Hay, I.D., Herrmann, M.A., Wu, P.S-C., Hay, I.D., Herrmann, M.A., Katzmann, J.A., Bergstralh, E.J., Herrera, M.F., Grant, C.S., Goellner, J.R.: Papillary thyroid carcinoma (PTC), oxyphilic cell type: A tumour misclassified by the World Health Organization (abstract). Clin. Res.39:279A, 1991
Kaplan, E.L., Meier, P.: Non-parametric estimation from incomplete observations. J. Am. Stat. Assoc.53:457, 1958
Peto, R., Pike, M.C., Armitage, P., Peto, R., Pike, M.C., Armitage, P., Breslow, N.E., Cox, D.R., Howard, S.V., Mantel, N., McPherson, K., Peto, J., Smith, P.G.: Design and analysis of randomized clinical trials requiring prolonged observation of each patient. II. Analysis and examples. Br. J. Cancer35:1, 1977
Smith, S.A., Hay, I.D., Goellner, J.R., Smith, S.A., Hay, I.D., Goellner, J.R., Ryan, J.J., McConahey, W.M.: Mortality from papillary thyroid carcinoma. A case control study of 56 lethal cases. Cancer62:1381, 1988
Ryan, J.J., Hay, I.D., Grant, C.S., Ryan, J.J., Hay, I.D., Grant, C.S., Rainwater, L.M., Farrow, G.M., Goellner, J.R.: Flow cytometric DNA measurements in benign and malignant Hürthle cell tumours of the thyroid. World J. Surg.12:482, 1988
Hay, I.D.: Cytometric DNA ploidy analysis in thyroid cancer. Diagn. Oncol.1:181, 1991
Hay, I.D., Grant, C.S., Taylor, W.F., Hay, I.D., Grant, C.S., Taylor, W.F., McConahey, W.M.: Ipsilateral lobectomy versus bilateral lobar resection in papillary thyroid carcinoma: A retrospective analysis of surgical outcome using a novel prognostic scoring system. Surgery102:1088, 1987
Tscholl-Ducommun, J., Hedinger, C.E.: Papillary thyroid carcinomas: Morphology and prognosis. Virchows Arch. [Pathol. Anat.]396:19, 1982
Sobrinho-Simoes, M.A., Nesland, J.M., Holm, R.: Hürthle cell and mitrochondrion-rich papillary carcinoma of the thyroid gland: An ultrastructural and immunocytochemical study. Ultrastruct. Pathol.8:131, 1985
Gonzalez-Campora, R., Herrero-Zapatero, A., Lerma, E., Gonzalez-Campora, R., Herrero-Zapatero, A., Lerma, E., Sanchez, F., Galera, H.: Hürthle cell and mitochondria-rich tumours. Cancer57:1154, 1986
Hill, J.H., Werkhaven, J.A., DeMay, R.M.: Hürthle cell variant of papillary carcinoma of the thyroid gland. Otolaryngol. Head Neck Surg.98:338, 1988
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Herrera, M.F., Hay, I.D., Wu, P.S.C. et al. Hürthle cell (oxyphilic) papillary thyroid carcinoma: A variant with more aggressive biologic behavior. World J. Surg. 16, 669–674 (1992). https://doi.org/10.1007/BF02067351
Issue Date:
DOI: https://doi.org/10.1007/BF02067351