Annals of Surgical Oncology Cite Track
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
10.1245/ASO.2006.03.062
Annals of Surgical Oncology 13:176-181 (2006)
© 2006 Society of Surgical Oncology
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lam, A. K. Y.
Right arrow Articles by Lo, C. Y.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lam, A. K. Y.
Right arrow Articles by Lo, C. Y.

Original Article

Diffuse Sclerosing Variant of Papillary Carcinoma of the Thyroid: A 35-Year Comparative Study at a Single Institution

Alfred King Yin Lam, MBBS, MD, FRCPA1 and Chung Yau Lo, MBBS, MS, FRCS (Edin), FACS2

1 Discipline of Pathology, School of Medicine, Gold Coast Campus, Griffith University, PMB 50 Gold Coast Mail Centre, Queensland, 9726, Australia
2 Department of Surgery, Faculty of Medicine, University of Hong Kong, Hong Kong

Correspondence: Address correspondence and reprint requests to: Alfred King Yin Lam, MBBS, MD, FRCPA; E-mail: a.lam{at}griffith.edu.au.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Diffuse sclerosing variant (DSV) is a rare variant of papillary thyroid carcinoma (PTC), and the features of this carcinoma have not been fully characterized. The aim of this study was to analyze the clinicopathologic features of a large cohort of patients with this disease.

Methods: We reclassified primary thyroid carcinomas treated in a 35-year study period and studied the clinicopathologic features and outcomes of DSV of PTC in comparison with classic PTC.

Results: Fifteen patients (2 men and 13 women) with DSV of PTC were identified who had surgical resection of the thyroid. Fine-needle aspiration biopsy diagnosed 83% (10 of 12) of the tumors. Compared with classic PTC, patients with DSV presented at a younger age (mean age, 29 vs. 46 years; P = .0001), had larger tumors (mean diameter, 3.6 vs. 2.2 cm; P = .002), and had a higher incidence of cervical nodal metastases (80% vs. 43%; P = .006). Ten patients had received postoperative iodine 131 ablation, and four had also received external-beam irradiation. Distant metastases were detected in two patients (one in lung and one in brain). One third (5 of 15) of the patients developed disease recurrence. Lymph node recurrence was detected in one patient 12 years after the initial operation. Over a median follow-up period of 10.7 years, one patient with an initial incomplete excision died of the carcinoma. The overall disease-specific survival rate was 93%.

Conclusions: DSV of PTC had distinctive clinicopathologic features and a high incidence of recurrence after operation but had a prognosis similar to that of classic PTC.

Key Words: Thyroid • Diffuse sclerosing variant • Papillary carcinoma • Prognosis • Clinicopathologic features


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In 1985, Vickery et al.1 described a new variant of papillary thyroid carcinoma (PTC), for which they proposed the term diffuse sclerosis. Diffuse sclerosing variant (DSV) of PTC is an uncommon variant of PTC that shows diffuse involvement of the thyroid, dense sclerosis, extensive squamous metaplasia, patchy to dense lymphocytic infiltrate, numerous psammoma bodies, and marked lymphatic permeation during histological examination. Survival data from the literature for patients with DSV are derived mainly from case reports and small reported series.2–35 The clinical behavior of this variant of PTC remains uncertain.

To determine the characteristic features of DSV of PTC, we reclassified all the primary thyroid tumors reported over the past 30 years in a tertiary referral hospital to discover cases with histological features of this variant. This study is one of the largest series of patients with this disease entity and has the longest mean follow-up in the literature.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The pathology slides of the patients with thyroid carcinoma diagnosed in Queen Mary Hospital from 1968 to 2002 were reviewed and reclassified with reference to the criteria defined by the World Health Organization classification of malignant tumors.36 Patients with thyroid tumors that had features of DSV of PTC were selected for further study. The main clinical and pathologic differential diagnoses of DSV of PTC were multifocal PTC and Hashimoto’s thyroiditis. The presence of numerous psammoma bodies, squamous metaplasia, and marked sclerosis were used as criteria to distinguish DSV from multifocal PTC. In addition, the characteristic nuclear features of papillary carcinoma distinguish the tumor from Hashimoto’s thyroiditis.

The clinical presentation, preoperative fine-needle aspiration, surgical treatment, postoperative adjuvant therapy, recurrence, and long-term survival of the patients with DSV of PTC were studied. The location, size, and histological features of the tumors were noted on pathologic examination.

In the same period, 815 PTCs were diagnosed in the hospital. Of these, 287 were classic PTC. The clinicopathologic features of DSV of PTC were compared with the 287 classic PTCs diagnosed in the same period.

All data were retrieved from the thyroid cancer computer database and re-entered after histological review. Statistical analysis was performed with Student’s t-test with the Yates correction for continuous variables and with the {chi}2 test or Fisher’s exact test for categorical variables. The significance level was taken at P < .05. Statistical analysis was performed with SPSS for Windows (version 12.0; SPSS Inc., Chicago, IL).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
There were 15 patients (2 men and 13 women) with DSV of PTC (Table 1Go). The mean age of these patients was 29 years (range, 10–57 years; SE, 11 years). Sixty percent (n = 9) of the patients were younger than 30 years. The variant accounted for 15 (1.8%) of 815 PTCs diagnosed over the 35-year study period. All patient presented with a clinically detectable neck mass. In addition, patients had associated symptoms at presentation, including hoarseness (n = 2), pressure effect (n = 1), clinically detectable cervical lymph nodes (n = 2), and distant metastasis (n = 1). The median duration of neck mass before presentation was 5 months (range, 1–240 months).


View this table:
[in this window]
[in a new window]
  		TABLE 1. Clinicopathologic features of diffuse sclerosing variant of papillary thyroid carcinoma
 
Fine-needle aspiration was performed in 12 patients for preoperative diagnosis. In 10 of these 12 patients, diagnosis of PTC was confirmed before operation. Numerous psammoma bodies were noted in the aspirates of nine patients, although the tumors were diagnosed as classic PTC on fine-needle aspiration biopsies. The fine-needle biopsy specimens of the other two patients showed no evidence of malignancy. Preoperative neck ultrasonography was pre-formed in seven patients.

Surgical treatment included total thyroidectomy (n = 11), near-total thyroidectomy (1 g of residual thyroid tissue remained; n = 3), and lobectomy (n = 1). Modified radical lymph node dissection was performed in 10 patients. Patients were selected for the lymph node dissection if they had (1) clinically detectable lymph nodes; (2) suspicious lymph nodes noted on preoperative ultrasonography; and (3) lymph nodes found during active intraoperative sampling. Ten patients, all with recently diagnosed disease, had received postoperative iodine 131 ablation, and four also received external-beam irradiation.

The tumor was at the left lobe (n = 7), the right lobe (n = 5), both lobes (n = 2), or the isthmus (n = 1) at presentation. The mean diameter of the lesion was 3.6 cm (range, 1.5–6 cm; SE, 3 cm). Diffuse sclerosis, lymphocyte and plasma cell infiltration, multiple small islands of PTC, and psammoma bodies were noted in all tumors. Calcification other than psammoma bodies was noted in six tumors. In the 57-year-old female patient with a 12-year history of goiter, osseous metaplasia (bone) was noted in the stroma of the PTC. Lymph node metastases were documented histologically in 12 (80%) of 15 patients at the time of thyroidectomy. A 31-year-old woman had radiological evidence (chest radiograph and computed tomographic scan) of multiple lung nodules at presentation. She underwent total thyroidectomy, lymph node excision, and two courses of postoperative radioiodine. The chest radiograph on follow-up was negative for metastases. She was alive and disease free for 11 years after the operation.

Compared with the cohort of 287 classic PTCs managed during the same period, patients with the sclerosing variant presented at a younger age (mean age, 29 vs. 46 years; P = .0001), had a larger tumor (mean size 3.6 vs. 2.6 cm; P = .002), and had a higher incidence of lymph node metastases (80% vs. 43%; P = .006). Although there seems to be a higher female preponderance for DSV when compared with classic PTC (male:female ratio, 1:6.5 vs. 1: 3.5), the difference was not statistically significant (P = .536).

One third (5 of 15) of the patients with DSV of PTC developed disease recurrence during follow-up. Four of these patients had local lymph nodal recurrence soon after the operation (mean, 11 months; range, 2–16 months). In all these patients, preoperative ultrasonography had been performed. In a 23-year-old woman, lymph node recurrence developed 12 years after the initial lobectomy. She then underwent a functional neck dissection and completion total thyroidectomy for the recurrence. She was alive without evidence of disease 3 years after the reoperation. There was no correlation between the occurrence of disease recurrence and the age or sex of patients, the duration of symptoms, the size of the tumor, or the presence of lymph node metastasis.

The mean and median follow-up period for patients with DSV of PTC was 10.7 and 12.5 years, respectively (range, 1.5–28.5 years). All patients but one were alive without evidence of disease at the last follow-up. The 10-year overall survival was 100%, and the overall cause-specific survival rate was 93%. The only mortality occurred in a 57-year-old woman who presented with a left thyroid mass, cervical lymph node, and left vocal cord palsy. Excision was incomplete; tumor was left at the tracheoesophageal groove. Despite administration of postoperative external irradiation and multiple courses of radioactive iodine ablation, her thyroglobulin increased 4 years after the operation. She presented with neurological symptoms and brain metastases 9.5 years after the initial operation and died of bronchopneumonia 1 year later (10.4 years after the initial presentation).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
To date, there were up to 150 cases of DSV of PTC reported in the literature.1–3 DSV of PTC is an uncommon pathologic entity, and, therefore, many of the cases were documented as case reports. The prevalence of this variant among all patients with PTC, as reported in larger series, ranged from .74% to 5.3%.33 Similarity to the findings in the literature, our study confirmed that this variant was uncommon and accounted for only 1.8% of all PTC cases.

Patients with DSV of PTC were frequently reported to be younger than patients with classic PTC.1–3 In the literature, the mean age reported for this variant (in series with more than five patients) ranged from 19.5 to 34.7 years. The youngest patient reported was 9 years old, and the oldest reported was 67 years old. In this series, the disease was seen at an age ranging from 10 to 57 years. Compared with classic PTC, patients with DSV presented at a younger age (mean age, 29 vs. 46 years). In addition, in reviewing the literature together with our own series, this variant tended to occur more frequently in women, similarly to classic PTC, and the clinical presentation of both types was also similar.

Fine-needle aspiration biopsy of thyroid nodules has proven to be sensitive, specific, and well accepted by patients because of minimal discomfort and complications.37 In this series, the sensitivity of diagnosis of the DSV of PTC by fine-needle aspiration was high, because 83% (10 of 12) of the tumors were diagnosed before operation. The sensitivity was higher than in diagnosis of PTC in general.38,39 This may be related to the diffuse involvement of the thyroid and the presence of numerous psammoma bodies in this variant of PTC. The presence of numerous psammoma bodies in the aspirate may help in identifying the DSV of PTC. Early diagnosis in these cases can assist clinicians with planning of management of this locally aggressive disease.

Histologically, DSV of PTC is characterized by diffuse involvement of one or both lobes of the thyroid gland associated with dense fibrosis, lymphatic infiltrate, multiple foci of squamous metaplastic changes, and numerous psammoma bodies. These features are present in all the cases in this series. In addition, osseous metaplasia was noted in one tumor. We have previously reported a high incidence of calcification/ossification in the stroma of the more aggressive thyroid carcinomas, insular and anaplastic thyroid carcinomas.40 In this series, osseous metaplasia was present in the patient with DSV of PTC who eventually died of the disease. It is likely that the presence of osseous metaplasia reflects the longstanding nature of the disease and can correlate with aggressive tumor behavior.

In this study, the sclerosing variant was found to be associated with unfavorable histological factors at the time of presentation. Compared with classic PTC, patients with the sclerosing variant presented at a younger age (mean age, 29 vs. 46 years), had larger tumors (mean diameter, 3.6 vs. 2.2 cm), and had a higher incidence of lymph node metastases (80% vs. 43%). In addition, disease recurrence was frequent, and delayed disease recurrence could occur up to 12 years after the initial operation. Thus, initial radical surgery followed by radioiodine treatment may be justified, and long-term follow-up is required for this group of patients. Preoperative neck ultrasonography may be helpful in detecting the presence of lymph node metastases in this disease entity. More importantly, an active search for suspicious lymph nodes should be performed at the initial operation if there is a clinicopathologic suggestion of the disease entity. Modified radical lymph node dissection could be performed if positive lymph nodes were found.

Distant metastasis is relatively uncommon in PTC; lung and bone are the most frequent sites of distant spread.41 As with the classic variant, the lung is the most common reported site of distant metastasis in DSV of PTC. All except two cases of DSV of PTC with distant metastases were noted in the lungs. In the literature, the reported incidence of distant metastases in DSV of PTC varies, with an average incidence of 14.9%.33 In this series, a similar incidence of 13% distant metastases was noted.

Brain metastases are extremely rare in PTC, with an incidence of <2%.41–43 In many instances, the interval between primary diagnosis of PTC and the occurrence of brain metastasis was usually within 5 years. Nevertheless, Paker et al.44 reported a patient with brain metastases 35 years after the diagnosis of PTC. In DSV of PTC, the only case of brain metastasis was reported in a 53-year-old Japanese man. The metastatic brain lesions presented before the diagnosis of the primary thyroid carcinoma.28 In this series, brain metastasis was noted in a 57-year-old Chinese woman 9.5 years after thyroidectomy for the primary tumor, and the patient died shortly afterward. Thus, brain metastasis could occur in DSV of PTC with lethal consequences.

It has been difficult to draw definite conclusions from the literature regarding the clinical behavior of DSV of PTC, partly because of the short and incomplete follow-up in many studies1–3 (Table 2Go). In some earlier reported series, patients with DSV were reported to have an unfavorable prognosis simply on the basis of the frequent occurrence of adverse pathologic features present in the limited number of cases. However, in many of these series, no mortality was reported. This study, when compared with the other studies on this variant of PTC, had very good long-term follow-up (median, 10.7 years; mean, 11.6 years). In our previous study on the same population, the 10-year survival rate for patients with PTC was 92%.45 In this study, the 10-year disease-specific survival was 93% for patients with DSV of PTC. Thus, it was appropriate to conclude that the prognosis of the patients with DSV of PTC seemed to be as favorable as that with classic PTC. The aggressive treatment protocol may account for the relatively good outcome despite the presence of unfavorable pathologic features at presentation and the high incidence of recurrence.


View this table:
[in this window]
[in a new window]
  		TABLE 2. Summary on the series on diffuse sclerosing variant of papillary thyroid carcinoma with follow-up information
 
In conclusion, our study showed that DSV of PTC, albeit rare, had clinicopathologic features distinct from those of classic PTC. The prognosis of the disease seems to be as good as that of classic PTC after complete surgical treatment and postoperative radioiodine ablation. Close follow-up was necessary because of the frequent tumor recurrence and the association with unfavorable pathologic features.

Received for publication March 8, 2005. Accepted for publication August 11, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Vickery AL Jr, Carcangiu ML, Johannessen JV, Sobrinho-Simoes M. Papillary carcinoma. Semin Diagn Pathol 1985;2: 90–100.[Medline]
  2. Matias-Guiu X, Esquius J. Aberrant expression of HLA-DR antigen in diffuse sclerosing variant of papillary carcinoma of thyroid. J Clin Pathol 1989;42:1309.[Free Full Text]
  3. Carcangiu ML, Bianchi S. Diffuse sclerosing variant of papillary thyroid carcinoma. Clinicopathologic study of 15 cases. Am J Surg Pathol 1989;13:1041–9.[Medline]
  4. Wu PS, Leslie PJ, McLaren KM, Toft AD. Diffuse sclerosing papillary carcinoma of thyroid: a wolf in sheep’s clothing. Clin Endocrinol 1989;31:535–40.[Medline]
  5. Soares J, Limbert E, Sobrinho-Simoes M. Diffuse sclerosing variant of papillary thyroid carcinoma. A clinicopathologic study of 10 cases. Pathol Res Pract 1989;185:200–6.[Medline]
  6. Caruso G, Tabarri B, Lucchi I, Tison V. Fine needle aspiration cytology in a case of diffuse sclerosing carcinoma of the thyroid. Acta Cytol 1990;34:352–4.[Medline]
  7. Chan JK. Papillary carcinoma of thyroid: classical and variants. Histol Histopathol 1990;5:241–57.[Medline]
  8. Fujimoto Y, Obara T, Ito Y, Kodama T, Aiba M, Yamaguchi K. Diffuse sclerosing variant of papillary carcinoma of the thyroid. Clinical importance, surgical treatment, and follow-up study. Cancer 1990;66:2306–12.[CrossRef][Medline]
  9. Mizukami Y, Nonomura A, Michigishi T, et al. Diffuse sclerosing variant of papillary carcinoma of the thyroid: report of three cases. Acta Pathol Jpn 1990;40:676–82.[Medline]
  10. Hayashi Y, Sasao T, Takeichi N, Kuma K, Katayama S. Diffuse sclerosing variant of papillary carcinoma of the thyroid: a histopathological study of four cases. Acta Pathol Jpn 1990;40:193–8.[Medline]
  11. Schroder S, Bay V, Dumke K, et al. Diffuse sclerosing variant of papillary thyroid carcinoma. S-100 protein immunocytochemistry and prognosis. Virchows Arch A Pathol Anat Histopathol 1990;416:367–71.[Medline]
  12. Gomez-Morales M, Alvaro T, Munoz M, et al. Diffuse sclerosing papillary carcinoma of the thyroid gland: immunohistochemical analysis of the local host immune response. Histopathology 1991;18:427–33.[Medline]
  13. Alejo M, Peiro G, Oliva E, Matias-Guiu X. Leu-M 1 immunoreactivity in papillary carcinomas of the thyroid gland; microcarcinoma, encapsulated, conventional and diffuse sclerosing subtypes. Virchows Arch A Pathol Anat Histopathol 1991;419:447–8.[Medline]
  14. Macak J, Michal M. Diffuse sclerosing variant of papillary thyroid carcinoma. Cesk Patol 1993;29:6–8.[Medline]
  15. Moreno Egea A, Rodriguez Gonzalez JM, Sola Perez J, Soria T, Parrilla Paricio P. Clinicopathological study of the diffuse sclerosing variety of papillary cancer of the thyroid: presentation of 4 new cases and review of the literature. Eur J Surg Oncol 1994;20:7–11.[Medline]
  16. Nikiforov Y, Gnepp DR. Pediatric thyroid-cancer after the Chernobyl disaster. Pathomorphologic study of 84 cases (1991–1992) from the Republic of Belarus. Cancer 1994; 74:748–66.[CrossRef][Medline]
  17. Damiani S, Dina R, Eusebi V. Cytologic grading of aggressive and nonaggressive variants of papillary thyroid carcinoma. Am J Clin Pathol 1994;101:651–5.[Medline]
  18. Scott GC, Meier DA, Dickinson CZ. Cervical lymph node metastasis of thyroid papillary carcinoma imaged with fluorine-18-FDG, technetium-99m-pertechnetate and iodine-131-sodium iodide. J Nucl Med 1995;36:1843–5.[Abstract/Free Full Text]
  19. Caplan RH, Wester S, Kisken AW. Diffuse sclerosing variant of papillary thyroid carcinoma: case report and review of the literature. Endocr Pract 1997;3:287–92.[Medline]
  20. Lloyd RV, Ferreiro JA, Jin L, Sebo TJ. TGFB, TGFB receptors, Ki-67, and p27(Kip)l expression in papillary thyroid carcinomas. Endocr Pathol 1997;8:293–300.[Medline]
  21. Martin-Perez E, Larranaga E, Serrano P. Diffuse sclerosing variant of papillary carcinoma of the thyroid. Eur J Surg 1998;164:713–5.[Medline]
  22. Kumarasinghe MP. Cytomorphologic features of diffuse sclerosing variant of papillary carcinoma of the thyroid: a report of two cases in children. Acta Cytol 1998;42:983–6.[Medline]
  23. Albareda M, Puig-Domingo M, Wengrowicz S, et al. Clinical forms of presentation and evolution of diffuse sclerosing variant of papillary carcinoma and insular variant of follicular carcinoma of the thyroid. Thyroid 1998;8:385–91.[Medline]
  24. Khan AR, Abu-Eshy SA. Variants of papillary carcinoma of the thyroid: experience at Asir Central Hospital. J R Coll Surg Edinb 1998;43:20–5.[Medline]
  25. Trovato M, Villari D, Bartolone L, et al. Expression of the hepatocyte growth factor and c-met in normal thyroid, non-neoplastic, and neoplastic nodules. Thyroid 1998;8:125–31.[Medline]
  26. Muzaffar M, Nigar E, Mushtaq S, Mamoon N. The morphological variants of papillary carcinoma of the thyroid: a clinico-pathological study—AFIP experience. Armed Forces Institute of Pathology. J Pak Med Assoc 1998;48:133–7.[Medline]
  27. Ohori NP, Schoedel KE. Cytopathology of high-grade papillary thyroid carcinomas: tall-cell variant, diffuse sclerosing variant, and poorly differentiated papillary carcinoma. Diagn Cytopathol 1999;20:19–23.[Medline]
  28. Imamura Y, Kasahara Y, Fukuda M. Multiple brain metastases from a diffuse sclerosing variant of papillary carcinoma of the thyroid. Endocr Pathol 2000;11:97–108.[Medline]
  29. Santoro M, Thomas GA, Vecchio G, et al. Gene rearrangement and Chernobyl related thyroid cancers. Br J Cancer 2000;82:315–22.[CrossRef][Medline]
  30. Kebapci N, Efe B, Kabukcuoglu S, Akalin A, Kebapci M. Diffuse sclerosing variant of papillary thyroid carcinoma with primary squamous cell carcinoma. J Endocrinol Invest 2002;25:730–4.[Medline]
  31. Marchesi M, Biffoni M, Biancari F, Berni A, Campana FP. Predictors of outcome for patients with differentiated and aggressive thyroid carcinoma. Eur J Surg Suppl 2003;588:46–50.
  32. Triggiani V, Ciampolillo A, Maiorano E. Papillary thyroid carcinoma, diffuse sclerosing variant, with abundant psammoma bodies. Acta Cytol 2003;47:1141–3.[Medline]
  33. Chow SM, Chan JK, Law SC, et al. Diffuse sclerosing variant of papillary thyroid carcinoma—clinical features and outcome. Eur J Surg Oncol 2003;29:446–9.[Medline]
  34. Borson-Chazot F, Causeret S, Lifante JC, Augros M, Berger N, Peix JL. Predictive factors for recurrence from a series of 74 children and adolescents with differentiated thyroid cancer. World J Surg 2004;28:1088–92.[CrossRef][Medline]
  35. Hirokawa M, Kuma S, Miyauchi A, et al. Morules in cribri-form-morular variant of papillary thyroid carcinoma: immunohistochemical characteristics and distinction from squamous metaplasia. APMIS 2004;112:275–82.[CrossRef][Medline]
  36. LiVolsi VA, Albores-Saavedra J, Asa SL, et al. (2004) Papillary carcinoma. In: DeLellis RA, Llyod RV, Heitz PU, Eng C (eds). World Health Organization Classification of Tumours: Pathology and Genetics—Tumours of Endocrine Organs International Agency for Research on Cancer, Lyon, pp 57–66.
  37. Baloch ZW, LiVolsi VA. Fine-needle aspiration of thyroid nodules: past, present, and future. Endocr Pract 2004;10:234–41.[Medline]
  38. Furlan JC, Bedard YC, Rosen IB. Role of fine-needle aspiration biopsy and frozen section in the management of papillary thyroid carcinoma subtypes. World J Surg 2004;28:880–5.[CrossRef][Medline]
  39. Gupta S, Sodhani P, Jain S, Kumar N. Morphologic spectrum of papillary carcinoma of the thyroid: role of cytology in identifying the variants. Acta Cytol 2004;48:795–800.[Medline]
  40. Lam KY, Lo CY, Chan KW, Wan KY. Insular and anaplastic carcinoma of the thyroid: a 45-year comparative study at a single institution and a review of the significance of p53 and p21. Ann Surg 2000;231:329–38.[CrossRef][Medline]
  41. Hoie J, Stenwig AE, Kullmann G, Lindegaard M. Distant metastases in papillary thyroid cancer: a. review of 91 patients. Cancer 1988;61:1–6.[CrossRef][Medline]
  42. Carcangiu ML, Zampi G, Pupi A, Castagnoli A, Rosai J. Papillary carcinoma of the thyroid: a. clinicopathologic study of 241 cases treated at the University of Florence, Italy. Cancer 1985;55:805–28.[CrossRef][Medline]
  43. McConahey WM, Hay ID, Woolner LB, van Heerden JA, Taylor WF. Papillary thyroid cancer treated at the Mayo Clinic, 1946 through 1970: initial manifestations, pathologic findings, therapy, and outcome. Mayo Clin Proc 1986;61:978–96.[Medline]
  44. Paker LN, Wu SY, Kim DD, Kollin J, Prasasvinichai S. Recurrence of papillary thyroid carcinoma presenting as a focal neurologic deficit. Arch Intern Med 1986;146:1985–7.[Abstract]
  45. Lorentz TG, Lau PW, Lo CY, Law WL, Wan KY, Lauder IJ. Multivariate analysis of risk factors influencing survival in 110 ethnic Chinese with papillary thyroid cancer. World J Surg 1994;18:547–50.[Medline]



This article has been cited by other articles:


Home page
 Am. J. Roentgenol.Home page
J. Y. Kwak, E.-K. Kim, E. J. Son, M. J. Kim, K. K. Oh, J. Y. Kim, and K. I. Kim
Papillary Thyroid Carcinoma Manifested Solely as Microcalcifications on Sonography
Am. J. Roentgenol., July 1, 2007; 189(1): 227 - 231.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lam, A. K. Y.
Right arrow Articles by Lo, C. Y.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lam, A. K. Y.
Right arrow Articles by Lo, C. Y.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS