10.1245/ASO.2006.08.020
Annals of Surgical Oncology 13:859-863 (2006)
© 2006 Society of Surgical Oncology
Fine-Needle Aspiration Optimizes Surgical Management in Patients With Thyroid Cancer
David Y. Greenblatt, MD1,
Todd Woltman, MD1,
Josephine Harter, MD2,
James Starling, MD1,
Eberhard Mack, MD1 and
Herbert Chen, MD1
1 Department of Surgery, University of Wisconsin, Madison, H4/750 Clinical Science Center, 600 Highland Avenue, Madison, Wisconsin 53792, USA
2 Department of Pathology, University of Wisconsin, Madison, H4/750 Clinical Science Center, 600 Highland Avenue, Madison, Wisconsin 53792, USA
Correspondence: Address correspondence and reprint requests to: Herbert Chen, MD; E-mail: chen{at}surgery.wisc.edu.
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ABSTRACT
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Background: Fine-needle aspiration (FNA) is accurate in diagnosing papillary, medullary, and anaplastic thyroid cancer, as well as lymphoma. Although many surgeons routinely perform FNA before surgery, some question whether FNA influences operative management. Therefore, to determine whether FNA affects surgical management in patients with thyroid cancer, we reviewed our experience.
Methods: A total of 442 consecutive patients underwent thyroid surgery at 1 academic center. Of these, 411 had surgery for an index nodule in the absence of previous radiation or familial thyroid cancer. FNA, operative, and permanent histology findings were reviewed.
Results: The average patient age was 46 years, and 79% were female. A total of 211 patients (51%) had a preoperative FNA, and 71 (17%) had a final diagnosis of cancer. The sensitivity and specificity of FNA for thyroid cancer were 89% and 92%, respectively. In the FNA group, 1 (2.4%) of 41 patients with papillary thyroid cancer required completion thyroidectomy. In contrast, in the no-FNA group, 4 (40%) of 10 patients with papillary thyroid cancer required a second operation. No patient in the FNA group received thyroid resection for lymphoma, whereas three (100%) of three patients with lymphoma in the no-FNA group were treated surgically. A total of 98% of the FNA group, compared with 54% of the no-FNA group, received optimal surgical treatment for thyroid cancer.
Conclusions: FNA is a sensitive and specific test for the diagnosis of thyroid cancer, allowing definitive initial surgery and avoiding unnecessary procedures. Therefore, we recommend routine use of preoperative thyroid FNA, even in those patients in whom a resection is already planned.
Key Words: Thyroid neoplasms Thyroid lymphoma Thyroid surgery Fine-needle aspiration
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INTRODUCTION
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Einhorn and Franzen1 of Sweden described a new diagnostic technique in 1962 in the article titled Thin-Needle Biopsy in the Diagnosis of Thyroid Disease. Thyroid fine-needle aspiration (FNA) biopsy did not become widespread in the United States until the 1980s. The procedure, which is inexpensive and easily performed in the clinic, soon became an important tool in the evaluation of thyroid disease.
There is a large body of literature on the merits of FNA for the identification of thyroid malignancy.213 FNA is accurate in diagnosing papillary (PTC), medullary (MTC), and anaplastic thyroid cancer, as well as thyroid lymphoma. An FNA diagnosis of cancer allows the surgeon to plan a definitive initial operation for patients with PTC or MTC. Furthermore, patients with an FNA diagnosis of anaplastic cancer or lymphoma may avoid unnecessary surgery and proceed directly with medical therapy. For these reasons, most surgeons routinely perform FNA before thyroid surgery. However, some question whether FNA influences operative management.14 Therefore, to determine whether FNA affects surgical management in patients with thyroid cancer, we reviewed our experience.
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METHODS
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A review of the University of Wisconsin Hospital operative database identified 442 consecutive patients who underwent thyroid surgery from January 1995 to April 2001. Thirty-one patients were excluded from the study for the following reasons: previous thyroid surgery (18 patients), history of neck radiotherapy (2 patients), and history of a familial thyroid cancer syndrome (11 patients). For the remaining 411 patients, cytopathologic, operative, and histopathologic findings were reviewed.
FNA results were grouped into the following categories: none, indeterminate, benign, suspicious for follicular or Hürthle cell neoplasm (SF), suspicious for malignancy (SM), and malignant. FNAs described as indeterminate, unsatisfactory, and nondiagnostic were coded as indeterminate. A report containing the diagnosis benign, goiter, cyst, adenoma, or no evidence of malignancy was recorded as benign. FNA reports that were suspicious or atypical with features suggestive of follicular neoplasms or Hürthle cell neoplasms were coded as SF. FNAs that were suspicious for malignancy but with no mention of follicular or Hürthle cell neoplasms were coded as SM. FNAs read by the pathologist as unequivocally malignant were coded as malignant. These FNA results were reviewed by a single cytopathologist.
Permanent pathologic diagnoses were coded as malignant for any report of PTC, MTC, or follicular, Hürthle cell, or anaplastic thyroid carcinoma. Lymphomas and metastatic disease of the thyroid were also recorded as malignant. A size cutoff of 8 mm was used for PTCstumors
8 mm in diameter were coded as malignant true PTCs, and those < 8 mm were coded as benign. All other diagnoses were coded as benign, including adenoma, goiter, thyroiditis, Hürthle cell adenoma, and hyperplasia.
FNA results were compared with permanent histological examination results for determinations of sensitivity, specificity, and predictive value. For these calculations, benign and indeterminate FNAs were considered negative test results, SM and malignant results were considered positive, and SF results were disregarded. The use of preoperative FNA was a decision made by the surgeon.
Statistical analysis was performed by analysis of variance (SPSS; SPSS Inc., Chicago, IL). Significance was defined as a P value of <.05.
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RESULTS
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Of the 411 patients who underwent thyroid surgery, 211 (51%) had preoperative FNAs (FNA group), and 200 did not (no-FNA group). The two groups were similar in terms of average age and sex distribution (Table 1
).
A total of 55 (26.1%) patients in the FNA group had a final histopathologic diagnosis of cancer, compared with 16 (8.0%) in the no-FNA group (Table 1
). In both groups, PTC was the most common cancer diagnosis, followed by follicular thyroid cancer and smaller numbers of MTC, anaplastic thyroid cancer, cancer from distant organs metastatic to the thyroid gland, and thyroid lymphoma (Table 2
). For the detection of thyroid malignancy, the sensitivity of FNA was 88.6%, the specificity was 92.3%, positive predictive value was 84.8%, and negative predictive value was 94.4%.
In the FNA group, 1 (2.4%) of 41 patients with PTC required a completion thyroidectomy. In contrast, in the no-FNA group, 4 (40%) of 10 patients with PTC required reoperation for completion thyroidectomy. The difference was statistically significant.
In the FNA group, there were two patients with MTC. The diagnosis was made in both cases by FNA. The patients received total thyroidectomy, and neither patient required further surgical treatment. No patient in the no-FNA group had MTC.
None of the patients with thyroid lymphoma in the FNA group received thyroidectomy, whereas three (100%) of three in the no-FNA group did. This difference was also statistically significant.
The percentages of patients who had optimal surgical treatment for PTC, MTC, and thyroid lymphoma in the FNA and no-FNA groups were 98% and 54%, respectively (Table 3
). This difference was statistically significant. Optimal surgical treatment with one operation was defined as no unnecessary surgery for lymphoma and no need for completion thyroidectomy for PTC and MTC.
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DISCUSSION
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Many authors have recommended FNA as an important test for the evaluation of thyroid nodules.25,7 The technique is safe and conveniently performed in the office setting. FNA is of limited utility for the diagnosis of follicular thyroid cancer because it is unable to identify the hallmark features of malignancy, including vascular and capsular invasion.15 However, the technique is highly accurate in the diagnosis of PTC, MTC, and anaplastic carcinomas, as well as of thyroid metastases and lymphoma. The widespread adoption of FNA has led to a decrease in diagnostic thyroidectomy.
Identification of a thyroid malignancy allows the planning of definitive therapy, be it surgical, as for PTC and MTC, or nonsurgical, as for anaplastic carcinoma and thyroid lymphoma. Although many surgeons routinely perform FNA before thyroid surgery, some authors have questioned the value of the test in influencing surgical management. For example, the group at the Memorial Sloan-Kettering Cancer Center has reported that preoperative FNA has no direct effect on their selection of surgical procedure.14 Instead, they rely on known prognostic factors and intraoperative findings to plan and perform thyroid operations. In our experience, FNA is a valuable tool in planning the operative management of thyroid cancer. We present in this article our data for FNA in the diagnosis of PTC, MTC, and thyroid lymphoma.
PTC is the most common type of thyroid cancer. Although some controversy exists over the operative treatment of PTC, we recommend total thyroidectomy rather than lobectomy.16 Foci of PTC are found in both thyroid lobes in 35% to 85% of patients with PTC.1720 Up to 10% of PTC recurrences occur in the contralateral lobe if not initially resected.21 Although no study has demonstrated a survival difference, several retrospective studies have shown a reduction in the risk of local recurrence in patients treated with total thyroidectomy compared with lesser resections.2225 Removal of all thyroid tissue allows the use of radioiodine to detect and treat metastatic disease. Furthermore, thyroglobulin may be monitored as a marker of disease recurrence.
In this study, 42 (98%) of 43 patients with PTC or MTC in the FNA group were treated with total thyroidectomy as the initial operation. One patient (2%) in the FNA group required a completion thyroidectomy for PTC. This patient had preoperative FNA and intraoperative frozen-section biopsies that were both negative for PTC, but the final histopathologic diagnosis was PTC. By contrast, 40% of the patients with PTC in the no-FNA group required completion thyroidectomy. Thus, although completion thyroidectomy is not entirely eliminated in patients with preoperative FNA, the need is markedly lower. The need for a second operation results in an increased cumulative risk for complications such as bleeding,26 hypoparathyroidism,27 and recurrent laryngeal nerve injury,26,28,29 as well as increased cost and patient inconvenience. In our opinion, the patients who did not receive preoperative FNA and eventually required completion thyroidectomy for PTC received suboptimal surgical care.
Primary thyroid lymphoma (PTL) is an uncommon malignancy. It accounts for < 4% of all extranodal non-Hodgkins lymphomas and 5% of thyroid malignancies.3034 PTLs typically occur in middle-aged and older women and arise in the setting of autoimmune thyroiditis. The relative risk of a patient with lymphocytic thyroiditis developing lymphoma has been estimated to be 40 to 80 times greater than in the general population.3537
In the past, thyroid lymphoma was thought to be a form of anaplastic thyroid carcinoma, and it was treated with radical thyroid resection.30,3840 As the benefit of radiation and chemotherapy in PTL became evident, thyroidectomy became less common as a treatment, although other invasive procedures were still necessary to establish the diagnosis.31,34,4153 With the widespread adoption of FNA in the diagnosis of systemic lymphomas, several authors began to discuss whether the technique could be used for PTLs, thus obviating the need for any surgical intervention.43,47,54,55 Advances in immunophenotypical analysis, including flow cytometry and immunohistochemistry, have improved the accuracy of FNA in diagnosing thyroid lymphoma, thus making invasive surgical diagnostic procedures generally unnecessary.56
In this study, three patients (100%) with PTL in the no-FNA group underwent thyroid operations. Two had lobectomies, and one had a total thyroidectomy. Thyroid surgery was probably not of benefit for these patients. FNA, had it been performed, could have resulted in an earlier diagnosis of PTL, more rapid definitive therapy, and the avoidance of unnecessary surgery.
In some cases, however, the diagnosis of PTL cannot be made with noninvasive techniques. One patient in the FNA group received a final diagnosis of thyroid lymphoma. This patient underwent an FNA and a core needle biopsy, both of which were non-diagnostic. The patient was taken to the operating room for incisional biopsy, and frozen-section analysis was positive for lymphoma. No further resection was performed, and the patient was referred for medical treatment.
Our data demonstrate that FNA improves surgical outcomes in patients with thyroid cancer. In our series, 98% of the patients with PTC, MTC, and thyroid lymphoma received optimal surgical treatmentdefined as no need for completion thyroidectomy for PTC and MTC and as no unnecessary surgery for lymphomain the FNA group, compared with only 54% in the no-FNA group.
In conclusion, FNA is a sensitive and specific technique for the identification of thyroid malignancy and other diseases such as follicular neoplasms that require surgery. FNA is an important tool for the diagnosis of cancer, allowing definitive initial surgery for PTC and MTC and the avoidance of unnecessary operations for thyroid lymphoma. Therefore, we recommend routine use of preoperative thyroid FNA, even in patients in whom a resection is already planned.
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FOOTNOTES
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Presented at the 58th Annual Meeting of the Society of Surgical Oncology, Atlanta, Georgia, March 36, 2005.
Received for publication August 12, 2005.
Accepted for publication November 22, 2005.
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REFERENCES
|
|---|
- Einhorn J, Franzen S. Thin-needle biopsy in the diagnosis of thyroid disease. Acta Radiol 1962; 58:32136.
- Hamburger JI, Hamburger SW. Declining role of frozen section in surgical planning for thyroid nodules. Surgery 1985; 98:30712.[Medline]
- Kopald KH, Layfield LJ, Mohrmann R, Foshag LJ, Giuliano AE. Clarifying the role of fine-needle aspiration cytologic evaluation and frozen section examination in the operative management of thyroid cancer. Arch Surg 1989; 124:12014; discussion 12045.[Abstract]
- Paphavasit A, Thompson GB, Hay ID, et al. Follicular and Hurthle cell thyroid neoplasms. Is frozen-section evaluation worthwhile? Arch Surg 1997; 132:6748; discussion 67880.[Abstract]
- Chen H, Nicol TL, Udelsman R. Follicular lesions of the thyroid. Does frozen section evaluation alter operative management? Ann Surg 1995; 222:1016.[Medline]
- Chen H, Zeiger MA, Clark DP, Westra WH, Udelsman R. Papillary carcinoma of the thyroid: can operative management be based solely on fine-needle aspiration? J Am Coll Surg 1997; 184:60510.[Medline]
- Shemen LJ, Chess Q. Fine-needle aspiration biopsy diagnosis of follicular variant of papillary thyroid cancer: therapeutic implications. Otolaryngol Head Neck Surg 1998; 119:6002.[CrossRef][Medline]
- Boyd LA, Earnhardt RC, Dunn JT, Frierson HF, Hanks JB. Preoperative evaluation and predictive value of fine-needle aspiration and frozen section of thyroid nodules. J Am Coll Surg 1998; 187:494502.[CrossRef][Medline]
- Sabel MS, Staren ED, Gianakakis LM, Dwarakanathan S, Prinz RA. Use of fine-needle aspiration biopsy and frozen section in the management of the solitary thyroid nodule. Surgery 1997; 122:10216; discussion 10267.[CrossRef][Medline]
- Irish JC, van Nostrand AW, Asa SL, Gullane P, Rotstein L. Accuracy of pathologic diagnosis in thyroid lesions. Arch Otolaryngol Head Neck Surg 1992; 118:91822.[Abstract]
- Layfield LJ, Mohrmann RL, Kopald KH, Giuliano AE. Use of aspiration cytology and frozen section examination for management of benign and malignant thyroid nodules. Cancer 1991; 68:1304.[CrossRef][Medline]
- Rodriguez JM, Parrilla P, Sola J, et al. Comparison between preoperative cytology and intraoperative frozen-section biopsy in the diagnosis of thyroid nodules. Br J Surg 1994; 81:11514.[Medline]
- Chang HY, Lin JD, Chen JF, et al. Correlation of fine needle aspiration cytology and frozen section biopsies in the diagnosis of thyroid nodules. J Clin Pathol 1997; 50:10059.[Abstract/Free Full Text]
- Brooks AD, Shaha AR, DuMornay W, et al. Role of fine-needle aspiration biopsy and frozen section analysis in the surgical management of thyroid tumors. Ann Surg Oncol 2001; 8:92100.[Abstract/Free Full Text]
- Emerick GT, Duh QY, Siperstein AE, Burrow GN, Clark OH. Diagnosis, treatment, and outcome of follicular thyroid carcinoma. Cancer 1993; 72:328795.[CrossRef][Medline]
- Chen H, Udelsman R. Papillary thyroid carcinoma: justification for total thyroidectomy and management of lymph node metastases. Surg Oncol Clin North Am 1998; 7:64563.[Medline]
- Smith RR, Frazell EL, Caulk R, Holinger PH, Russell WO. The American Joint Committees proposed method of stage classification and end-result reporting applied to 1,320 pharynx cancers. Cancer 1963; 16:150520.[CrossRef][Medline]
- Katoh R, Sasaki J, Kurihara H, Suzuki K, Iida Y, Kawaoi A. Multiple thyroid involvement (intraglandular metastasis) in papillary thyroid carcinoma. A clinicopathologic study of 105 consecutive patients. Cancer 1992; 70:158590.[CrossRef][Medline]
- Pacini F, Elisei R, Capezzone M, et al. Contralateral papillary thyroid cancer is frequent at completion thyroidectomy with no difference in low- and high-risk patients. Thyroid 2001; 11:87781.[CrossRef][Medline]
- Kim ES, Kim TY, Koh JM, et al. Completion thyroidectomy in patients with thyroid cancer who initially underwent unilateral operation. Clin Endocrinol (Oxf) 2004; 61:1458.[CrossRef][Medline]
- Tollefsen HR, Decosse JJ. Papillary carcinoma of the thyroid. Recurrence in the thyroid gland after initial surgical treatment. Am J Surg 1963; 106:72834.[Medline]
- Hay ID. Papillary thyroid carcinoma. Endocrinol Metab Clin North Am 1990; 19:54576.[Medline]
- DeGroot LJ, Kaplan EL, McCormick M, Straus FH. Natural history, treatment, and course of papillary thyroid carcinoma. J Clin Endocrinol Metab 1990; 71:41424.[Abstract]
- Samaan NA, Schultz PN, Hickey RC, et al. The results of various modalities of treatment of well differentiated thyroid carcinomas: a retrospective review of 1599 patients. J Clin Endocrinol Metab 1992; 75:71420.[Abstract]
- Mazzaferri EL, Jhiang SM. Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med 1994; 97:41828.[CrossRef][Medline]
- Menegaux F, Turpin G, Dahman M, et al. Secondary thyroidectomy in patients with prior thyroid surgery for benign disease: a study of 203 cases. Surgery 1999; 126:47983.[Medline]
- Reeve TS, Delbridge L, Brady P, Crummer P, Smyth C. Secondary thyroidectomy: a twenty-year experience. World J Surg 1988; 12:44953.[CrossRef][Medline]
- Wilson DB, Staren ED, Prinz RA. Thyroid reoperations: indications and risks. Am Surg 1998; 64:6748; discussion 6789.[Medline]
- Chao TC, Jeng LB, Lin JD, Chen MF. Reoperative thyroid surgery. World J Surg 1997; 21:6447.[CrossRef][Medline]
- Compagno J, Oertel JE. Malignant lymphoma and other lymphoproliferative disorders of the thyroid gland. A clinicopathologic study of 245 cases. Am J Clin Pathol 1980; 74:111.[Medline]
- Doria R, Jekel JF, Cooper DL. Thyroid lymphoma. The case for combined modality therapy. Cancer 1994; 73:2006.[CrossRef][Medline]
- Tsang RW, Gospodarowicz MK, Sutcliffe SB, Sturgeon JF, Panzarella T, Patterson BJ. Non-Hodgkins lymphoma of the thyroid gland: prognostic factors and treatment outcome. The Princess Margaret Hospital Lymphoma Group. Int J Radiat Oncol Biol Phys 1993; 27:599604.[Medline]
- Staunton MD, Greening WP. Clinical diagnosis of thyroid cancer. Br Med J 1973; 4:5325.[Medline]
- Glass AG, Karnell LH, Menck HR. The National Cancer Data Base report on non-Hodgkins lymphoma. Cancer 1997; 80:231120.[CrossRef][Medline]
- Holm LE, Blomgren H, Lowhagen T. Cancer risks in patients with chronic lymphocytic thyroiditis. N Engl J Med 1985; 312:6014.[Abstract]
- Kato I, Tajima K, Suchi T, et al. Chronic thyroiditis as a risk factor of B-cell lymphoma in the thyroid gland. Jpn J Cancer Res 1985; 76:108590.[Medline]
- Pedersen RK, Pedersen NT. Primary non-Hodgkins lymphoma of the thyroid gland: a population based study. Histopathology 1996; 28:2532.[CrossRef][Medline]
- Campbell DJ, Sage RH. Thyroid cancer: twenty years experience in a general hospital. Br J Surg 1975; 62:20714.[Medline]
- Hamburger JI, Miller JM, Kini SR. Lymphoma of the thyroid. Ann Intern Med 1983; 99:68593.[Medline]
- Pasieka JL. Hashimotos disease and thyroid lymphoma: role of the surgeon. World J Surg 2000; 24:96670.[CrossRef][Medline]
- Laing RW, Hoskin P, Hudson BV, et al. The significance of MALT histology in thyroid lymphoma: a review of patients from the BNLI and Royal Marsden Hospital. Clin Oncol (R Coll Radiol) 1994; 6:3004.[CrossRef]
- Skarsgard ED, Connors JM, Robins RE. A current analysis of primary lymphoma of the thyroid. Arch Surg 1991; 126:1199203; discussion 12034.[Abstract]
- Pyke CM, Grant CS, Habermann TM, et al. Non-Hodgkins lymphoma of the thyroid: is more than biopsy necessary? World J Surg 1992; 16:6049; discussion 60910.[CrossRef][Medline]
- Aozasa K, Ueda T, Katagiri S, Matsuzuka F, Kuma K, Yonezawa T. Immunologic and immunohistologic analysis of 27 cases with thyroid lymphomas. Cancer 1987; 60:96973.[CrossRef][Medline]
- Rasbach DA, Mondschein MS, Harris NL, Kaufman DS, Wang CA. Malignant lymphoma of the thyroid gland: a clinical and pathologic study of twenty cases. Surgery 1985; 98:116670.[Medline]
- Junor EJ, Paul J, Reed NS. Primary non-Hodgkins lymphoma of the thyroid. Eur J Surg Oncol 1992; 18:31321.[Medline]
- Friedberg MH, Coburn MC, Monchik JM. Role of surgery in stage IE non-Hodgkins lymphoma of the thyroid. Surgery 1994; 116:10616; discussion 10667.[Medline]
- Vigliotti A, Kong JS, Fuller LM, Velasquez WS. Thyroid lymphomas stages IE and IIE: comparative results for radiotherapy only, combination chemotherapy only, and multimodality treatment. Int J Radiat Oncol Biol Phys 1986; 12:180712.[Medline]
- Connors JM, Klimo P, Fairey RN, Voss N. Brief chemotherapy and involved field radiation therapy for limited-stage, histologically aggressive lymphoma. Ann Intern Med 1987; 107:2530.[Medline]
- Sasai K, Yamabe H, Haga H, et al. Non-Hodgkins lymphoma of the thyroid. A clinical study of twenty-two cases. Acta Oncol 1996; 35:45762.[Medline]
- Devine RM, Edis AJ, Banks PM. Primary lymphoma of the thyroid: a review of the Mayo Clinic experience through 1978. World J Surg 1981; 5:338.[CrossRef][Medline]
- Ansell SM, Grant CS, Habermann TM. Primary thyroid lymphoma. Semin Oncol 1999; 26:31623.[Medline]
- Udelsman R, Chen H. The current management of thyroid cancer. Adv Surg 1999; 33:127.[Medline]
- Roeher HD, Simon D. Surgical therapy of thyroid cancer. G Chir 1999; 20:58.[Medline]
- Klyachkin ML, Schwartz RW, Cibull M, et al. Thyroid lymphoma: is there a role for surgery? Am Surg 1998; 64:2348.[Medline]
- Cha C, Chen H, Westra WH, Udelsman R. Primary thyroid lymphoma: can the diagnosis be made solely by fine-needle aspiration? Ann Surg Oncol 2002; 9:298302.[Abstract/Free Full Text]