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10.1245/s10434-006-9083-z
Annals of Surgical Oncology 14:712-718 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Surgical Treatment of Solitary Thyroid Nodules Via Fine-Needle Aspiration Biopsy and Frozen-Section Analysis

Tzu-Chieh Chao, MD, PhD1,4, Jen-Der Lin, MD2,5, Hsiao-Hsiang Chao, MD1, Chuen Hsueh, MD3,6 and Miin-Fu Chen, MD1,4

1 Department of Surgery, Division of General Surgery, Chang Gung Memorial Hospital at Linkou, 5 Fuhsing Street, Kweishan, Taoyuan, Taiwan
2 Department of Internal Medicine, Division of Metabolism and Endocrinology, Chang Gung Memorial Hospital at Linkou, 5 Fuhsing Street, Kweishan, Taoyuan, Taiwan
3 Department of Pathology, Chang Gung Memorial Hospital at Linkou, 5 Fuhsing Street, Kweishan, Taoyuan, Taiwan
4 Department of Surgery, Chang Gung University College of Medicine, 259 Wenhwa 1st Road, Kweishan, Taoyuan, Taiwan
5 Department of Internal Medicine, Chang Gung University College of Medicine, 59 Wenhwa 1st Road, Kweishan, Taoyuan, Taiwan
6 Department of Pathology, Chang Gung University College of Medicine, 59 Wenhwa 1st Road, Kweishan, Taoyuan, Taiwan

Correspondence: Address correspondence and reprint requests to: Tzu-Chieh Chao, MD, PhD; E-mail: tcchao{at}adm.cgmh.org.tw


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Fine-needle aspiration biopsy (FNAB) and frozen-section analysis of managing solitary thyroid nodules continue to generate considerable controversy.

Methods: This study was a retrospective review of 619 patients with solitary thyroid nodules who underwent thyroidectomy.

Results: Of 540 FNABs, 35 (6.5%) were positive for malignancy, 276 (51.1%) were benign, and 229 (42.4%) were suspicious. Only 5.1% were false negative, and 11.4% were false positive. Diagnostic FNAB sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and accuracy for malignancy were 86.1%, 59.7%, 33.0%, 94.9%, and 64.6%, respectively. Of 569 patients analyzed by frozen section, diagnosis was deferred in 86 (15.1%) patients, and results were positive for malignancy in 92 (16.2%) and benign in 391 (68.7%). No false-positive results were noted, but 2.3% (391) were false negative. Of 86 deferred frozen sections, 11 (12.8%) patients had malignant tumors confirmed by permanent section. Diagnostic frozen-section sensitivity, specificity, PPV, NPV, and accuracy for carcinoma were 82.1%, 100%, 100%, 95.8%, and 96.5%, respectively. Sensitivity, specificity, PPV, NPV, and accuracy for frozen-section analysis for diagnosis of carcinoma in patients with suspicious FNAB were 83.9%, 100%, 100%, 94.9%, and 96.0%, respectively.

Conclusions: FNAB is a sensitive diagnostic modality in selecting patients who require surgery. Routine use of frozen-section analysis is unwarranted for benign FNAB results. Frozen section is specific and cost-effective in determining the extent of surgery in patients with suspicious or malignant FNABs.

Key Words: Nodule • Fine-needle biopsy • Frozen section • Thyroid


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The prevalence of thyroid nodules, both solitary and multiple, is 4% to 7% in the general population.1 Overall, the incidence of malignant tumors reported in thyroid nodules is 5% to 30%.2,3 Thyroid cancer has been diagnosed in 0% to 11% of patients with multinodular goiters and in 3% to 33% of cases with solitary thyroid nodules.4 Preoperative identification of malignant tumors renders surgical planning straightforward. Clinical evaluation of nodule size, morphology, and function is very inaccurate for diagnosing malignancy. To determine the malignancy in thyroid nodules, fine-needle aspiration biopsy (FNAB) and frozen section are diagnostic modalities that have been used by many authors for preoperative or intraoperative nodule evaluation.

Some authors argue that FNAB is an effective preoperative examination for identifying malignancy5–7 and rely on intraoperative frozen section to determine the extent of operation.8–11 However, others argue that FNAB accuracy is sufficiently high to avoid intraoperative frozen section and thereby reduce operative time and cost.5,12–14 The controversies surrounding this issue in part result from most reports including both solitary and multinodular goiters. Obtaining a definite diagnosis in multinodular goiter by FNAB or frozen section can be difficult because other nodules can mask lesion pathology. This study evaluates preoperative FNAB and intra-operative frozen section to determine their relative efficacy in guiding surgical management of solitary thyroid nodules.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A total of 636 patients with ultrasonography-confirmed solitary thyroid nodules underwent thyroid surgery at Chang Gung Memorial Hospital between January 2002 and June 2004. Fourteen patients with multiple nodules determined by pathologic examination and three patients with incidental papillary microcarcinoma (tumor size, .1–.3 cm) were excluded. Data for the remaining 619 patients were retrospectively reviewed. Of these patients, 49 patients had FNAB performed at other hospitals and were excluded from FNAB analysis results. The remaining 570 patients had preoperative FNAB performed at Chang Gung Memorial Hospital. A total of 569 patients had intraoperative frozen sections. Of these patients, 522 patients had both preoperative FNAB and intraoperative frozen section. For frozen-section analysis, two representative sections including the tumor capsule and adjacent thyroid tissue were taken and frozen rapidly to –20°C in the cryostat. Subsequently, two frozen sections per block were cut and stained by a modified hematoxylin and eosin method. A diagnosis was made and called to the operating room within 20 minutes of receipt of the specimen.

FNAB results are considered malignant for diagnoses of thyroid cancer, lymphoma, or metastatic disease. Diagnoses of follicular neoplasm, Hürthle cell neoplasm, or possible or suspicious for follicular neoplasm or Hürthle cell neoplasm are recorded as follicular neoplasms. Follicular neoplasms and possible or suspicious diagnoses for any malignancy are coded as suspicious. Those reported as benign, cyst, goiter, nodule, adenoma, possible for any benign lesions, or no evidence of malignancy are categorized as benign. Frozen-section analysis results for the thyroid gland are coded as malignant for all thyroid cancers, lymphoma, or metastatic diseases. Goiter, hyperplasia, thyroiditis, and adenoma are considered benign. Reports of using "favor" or "possible" for any malignancy or suspicious for capsular invasion, follicular neoplasm, or Hürthle neoplasm are coded as deferred (defer reporting results until permanent sections are reported). Definite pathologic categorization is based on permanent-section diagnosis. Permanent histopathologic diagnoses are coded as malignant for papillary, follicular, Hürthle cell, medullary, poorly differentiated, and anaplastic thyroid carcinomas. Lymphoma and metastatic disease involving the thyroid gland are coded as malignant. All remaining diagnoses are coded as benign, including goiter, adenoma, hyperplasia, and thyroiditis.

For FNABs, lesions coded as suspicious are included in the malignant group, on the basis of its effects on surgical decisions. Conversely, deferred frozen-section samples are classified as benign, because surgery is typically terminated and further management is based on the permanent-section diagnosis. A true positive (TP) is a positive result for malignancy with subsequent final histopathologic verification. A true negative (TN) is a negative result for malignancy with subsequent final histopathologic confirmation. A false positive (FP) is a positive result for malignancy and benign results for the final his-topathologic diagnosis. A false negative (FN) is a reading consistent with benign disease and malignant on final histopathologic diagnosis. Sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and accuracy for detection of malignancy are determined for both FNAB and frozen-section analysis according to the following equations: sensitivity = TP/(TP + FN); specificity = TN/(TN + FP); PPV = TP/(TP + FP); NPV = TN/(TN + FN); and accuracy = (TP + TN)/(TP + TN + FP + FN).

Continuous data are expressed as mean ± SD unless otherwise stated. The unpaired t-test was used for continuous variables. Noncontinuous variables were analyzed for statistical significance by using {chi}2 analysis. P < .05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient age was 40.6 ± 13.5 years (range, 11–84 years). The age of patients with benign nodules was 40.4 ± 13.3 years (range, 13–78 years), and for those with malignant tumors, it was 41.7 ± 14.6 years (range, 11–84 years). Of the 619 patients, 529 (85.5%) were female and 90 (14.5%) were male. Of those with benign nodules, 433 were female and 71 were male; 96 females and 19 males had malignant tumors. Nodule size, as measured by ultrasonography, was 3.3 ± 1.2 cm (range, .7–6.5 cm). Benign nodule size, measured by ultrasonography, was 3.4 ± 1.2 cm (range, .7–6.5 cm), whereas malignant tumor size was 3.6 ± 1.2 cm (range, .8–6.0 cm). Pathologic tumor size was 3.1 ± 1.6 cm (range, .5–11.0 cm). The pathologic tumor size of benign nodules was 3.2 ± 1.5 cm (range, .5–11 cm), and that for malignant nodules was 2.5 ± 1.6 cm (range, .5–8.0 cm). Age, tumor size measured by ultrasonography, pathologic tumor size, and sex ratio were not significantly different between the benign and malignant groups. Two-hundred forty-three nodules were located at the left lobe, 353 at the right lobe, and 23 at the isthmus. The final his-topathologic diagnosis (Table 1Go) identified malignant tumors in 115 (18.6%) patients; papillary carcinoma was the most frequent diagnosis, seen in 90 (78.3%) patients with malignant tumors.


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  		TABLE 1. Permanent-section histopathologic examination in 619 patients
 
Unsatisfactory FNAB results for 30 (5.3%) patients were excluded from the analysis of FNAB results. These patients underwent thyroidectomy after they declined rebiopsy. The final diagnoses of those with unsatisfactory FNAB results comprised 27 benign nodules and 3 malignant tumors. Of the remaining 540 FNAB biopsies, 35 (6.5%) were malignant, 276 (51.1%) were benign, and 229 (42.4%) were suspicious (Table 2Go). Patients with benign FNAB diagnoses underwent operation because of pressure symptoms or unwillingness to carry out follow-up. Fourteen (5.1%) of 276 patients with benign FNAB results were FN. Four (11.4%) of 35 patients with malignant FNAB findings were FP. Of 32 cases with a FNAB diagnosis of papillary carcinoma, 29 (90.6%) were papillary carcinomas, 2 (6.3%) were nodular hyperplasias, and 1 (3.1%) was follicular adenoma. Moreover, 173 (75.6%) benign nodules and 56 (24.5%) malignant tumors in 229 patients had suspicious FNAB findings. The patients with suspicious FNAB lesions comprised 173 with diagnoses of follicular neoplasms and 56 with diagnoses suggestive of malignancy. Thirty (17.3%) of the patients with follicular neoplasms had malignancies, including 21 (70%) papillary carcinomas, 6 (20%) follicular carcinomas, 2 (6.7%) Hürthle cell carcinomas, and 1 (3.3%) metastatic carcinoma. Twenty-six (46.4%) of the patients with suggested malignancy on final histological analysis had malignant tumors, comprising 19 (73%) papillary carcinomas, 3 (11.5%) follicular carcinomas, 1 (3.9%) medullary carcinoma, 1 (3.9%) anaplastic carcinoma, 1 (3.9%) poorly differentiated carcinoma, and 1 (3.9%) plasmacytoma. To evaluate FNAB, suspicious was assigned to the malignant group because of its effect on surgical decisions. Sensitivity, specificity, PPV, NPV, and accuracy for FNAB in malignancy diagnosis were 86.1%, 59.7%, 33.0%, 94.9%, and 64.6%, respectively.


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  		TABLE 2. Histopathology in 540 patients undergoing pre-operative FNAB
 
Intraoperative frozen-section analysis for the thyroid was performed in 569 patients (Table 3Go). Of these, diagnosis was deferred in 86 (15.1%) patients, and results were positive for malignancy in 92 (16.2%) patients and benign in 391 (68.7%) patients. Nine (2.3%) diagnoses were FN in benign frozen sections; no FP malignant frozen-section findings were noted. Of 86 deferred frozen-section results, 11 (12.8%) cases had malignant tumors verified by permanent-section examinations. For assessment of frozen-section results, deferred frozen-section samples were classified as benign when surgery was terminated and further management was based on the permanent-section diagnosis. Sensitivity, specificity, PPV, NPV, and accuracy for frozen-section analysis in carcinoma diagnosis were 82.1%, 100%, 100%, 95.8%, and 96.5%, respectively.


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  		TABLE 3. Histopathology in 569 patients undergoing frozen-section analysis
 
After 26 patients with unsatisfactory FNAB results were excluded, data for the remaining 496 patients who had FNAB and frozen section were examined for relationships between FNAB, frozen-section analysis, and final histological diagnosis (Table 4Go). In the patient group with benign FNAB results, 12 (5.0%) had FN FNABs. Among these 12, 6 tumors were accurately diagnosed as malignant on frozen section, 4 were diagnosed as benign on frozen section as well, and 2 were deferred. In 223 patients with suspicious FNAB results, 47 tumors (21.1%) were malignant, 133 (59.6%) were benign, and 43 (19.3%) were deferred on frozen-section reports. Of these 223 patients, permanent-section analysis confirmed malignancy in 3 (2.2%) of 133 benign frozen sections and in 6 (12.8%) of 47 deferred frozen sections.


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  		TABLE 4. Permanent-section histopathology in 496 patients who received both FNAB and frozen-section analysis
 
Sensitivity, specificity, PPV, NPV, and accuracy for frozen-section analysis for carcinoma diagnosis in patients with suspicious FNAB findings were 83.9%, 100%, 100%, 94.9%, and 96.0%, respectively. Of these, 168 who had FNAB diagnoses of follicular neoplasm, Hürthle cell neoplasm, or possible or suspicious diagnoses for follicular neoplasm or Hürthle cell neoplasm underwent intraoperative frozen-section analysis. Sensitivity, specificity, PPV, NPV, and accuracy for frozen-section analysis for the diagnosis of carcinoma in these patients were 83.3%, 100%, 100%, 96.5%, and 97.0%, respectively. Sensitivity, specificity, PPV, NPV, and accuracy for frozen-section analysis in 55 patients with FNAB suggestive of malignancy were 84.6%, 100%, 100%, 87.9%, and 92.7%, respectively. Four (11.8%) of 34 patients with malignant FNAB had benign results on frozen section. Permanent-section diagnoses of these four patients comprised two nodular hyperplasias, one follicular adenoma, and one Hürthle cell adenoma.

Lobectomy with or without isthmusectomy was performed in 483 (78.0%) patients; total thyroidectomy, in 94 (15.2%) patients (including 10 completion thyroidectomies); total thyroidectomy and ipsilateral neck lymph node dissection, in 8 (1.3%) patients; subtotal thyroidectomy, in 6 (1.0%) patients; subtotal lobectomy, in 7 (1.1%) patients; isthmusectomy, in 17 (2.8%) patients; lobectomy and contralateral subtotal lobectomy, in 3 (.5%) patients; and near-total thyroidectomy, in 1 (.2%) patient. Permanent-section histological analysis revealed malignancy in 20 (4.2%) of 477 patients with benign or deferred frozen-section results. Ten of these patients underwent completion thyroidectomy. Another patient who initially underwent lobectomy and contralateral subtotal lobectomy did not undergo further operation. The remaining nine patients declined completion thyroidectomy. Six (2.5%) of 239 patients with benign FNAB findings and 47 (21.1%) of 223 patients with suspicious FNAB findings underwent total thyroidectomy on the basis of a malignant frozen-section diagnosis (Table 4Go). Furthermore, procedures for 4 (11.8%) of 34 patients with malignant FNAB results were terminated at lobectomy or lobectomy with isthmusectomy because of a benign frozen-section finding.

The cost of each frozen section was NT$ (New Taiwan dollar) 5612. The cost of repeat operation was estimated at NT$30,820 by averaging the cost for completion thyroidectomy in this series. The cost of routine frozen section in 496 patients who underwent both FNAB and frozen section was assessed by comparing the number of second operations needed with the reoperations required when frozen section was not performed. The total cost of frozen section in 496 operations was NT$2,786,528. Routine frozen section resulted in 15 reoperations at a total cost of NT$462,300. Surgical decisions based on FNAB only would have resulted in 68 reoperations at a total cost of NT$2,095,760. Routine use of frozen section in this series was estimated at an additional cost of NT$1,153,068. Because only 6 (2.5%) patients with a benign FNAB diagnosis had malignant tumors con-firmed by frozen section, the value of frozen section was analyzed as if it had been performed only in 223 patients with a suspicious FNAB diagnosis. In this case, the total cost of frozen section was NT$1,252,814, and this would have generated 21 reoperations at a total cost of NT$647,220. Routine use of frozen section limited to patients with a suspicious FNAB diagnosis led to an estimated savings of NT$195,726. Conversely, frozen section performed for patients with either a suspicious or a malignant FNAB diagnosis and not in those with benign FNAB findings resulted in an estimated savings of NT$4714.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The extent of thyroidectomy for well-differentiated thyroid cancers remains controversial. Some authors have suggested that procedures achieving less than near-total/total thyroidectomy are suited to well-differentiated thyroid cancers.15–18 Conversely, others—including the authors of this study—advocate near-total/total thyroidectomy for well-differentiated thyroid cancers.19–23 A repeat operation (completion thyroidectomy) is commonly performed for those with a definite diagnosis determined by permanent-section examination.21,23–25 Accurate preoperative or intra-operative diagnosis of malignancy by FNAB or frozen section can allow definitive surgery during the initial operation and eliminate the need for a second operation and the associated patient discomfort. A good diagnostic modality must be sufficiently sensitive for diagnosis of malignant tumors to select patients for operation and, conversely, have an adequately high specificity for determining the extent of operation. The sensitivity, specificity, PPV, NPV, and accuracy of FNAB vary when suspicious and/or follicular results are grouped with positive FNAB results or negative FNAB results or discounting them entirely. In this study, suspicious FNAB lesions were classified in the malignant group because of their effects on surgical decisions. FNAB for grouping suspicious lesions in the malignant group has a reported sensitivity of 69% to 88%, a specificity of 45% to 91%, a PPV of 28% to 71%, an NPV of 74% to 94%, and an accuracy of 53% to 86%.12,26–28 Our results for sensitivity (86.1%) and NPV (94.9%) and the FN rate (5.1%) indicate that an FNAB benign diagnosis is reliable for selecting patients who require operation; however, a negative FNAB should not be applied as confirmation when other clinical factors are indicative of malignancy. FN FNAB diagnoses are a concern for numerous researchers. The FN rate in this patient series is similar to that reported in literature, which varies from 1.3% to 26%.27,29–32 Sampling error for either big or small nodules or interpretive mistakes has been noted as the largest contributor to the FN fine-needle aspiration results.30,33,34 Some researchers recommend frozen section to verify malignancy.11 However, we do not recommend routine frozen section in cases of benign FNAB findings because it is not cost-effective and because only roughly 50% of nodules with an FN FNAB diagnosis can be demonstrated as malignant via intraoperative frozen section (Table 4Go).

The reported FP rate of FNAB was low (0%–2.5%).35 However, FNAB had an FP rate of 11.4% in this study. Two FP lesions were follicular adenoma and Hürthle cell adenoma verified by permanent-section examination. Sampling error and the cytologist’s ability may account for FP findings. For lesions with FP FNAB findings, lobectomy and removed frozen lesion sections should be used before total thyroidectomy is initiated, because frozen section can accurately diagnose such lesions (Table 4Go).

Generally, frozen section is considered to have enhanced specificity for diagnosing thyroid cancers. The sensitivity, specificity, PPV, NPV, and accuracy of frozen section reported in the literature are 57% to 80%, 98% to 99%, 95% to 97%, 74% to 95%, and 77% to 96%, respectively.26,27,36–38 In this study, 2.3% of cases diagnosed by frozen section as benign lesions were FN; however, malignant frozen-section diagnosis obtained no FPs (Table 3Go). Our findings indicate that frozen section is reliable in diagnosing benign and malignant tumors. Conversely, in 12.8% of those diagnosed as deferred frozen-section results, permanent-section examinations confirmed malignancy. Deferred frozen-section diagnoses are classified as benign in this study because surgery was terminated and further management was based on permanent-section diagnosis. In this scenario, frozen section had high specificity, PPV, and NPV rates—significantly higher than those for detection of a malignancy by using FNAB. High specificity, PPV, and NPV combine to make frozen section a specific diagnostic modality in planning the extent of operation and reducing the number of reoperations.

Diagnosis of follicular and Hürthle cell carcinomas is based on identifying tumor cell invasion in the capsule or vascular involvement.39,40 However, FNAB is unsuited to this goal, and only a diagnosis of follicular neoplasm or Hürthle cell neoplasm is appropriate. Some studies have proposed that frozen section is of little benefit with minimal diagnostic value, arguing that frozen section should be omitted in managing such lesions.12–14,41,42 However, others have recommended using frozen section to elucidate a suspicious, unsatisfactory, or absent FNAB result.8–11,43 In this study, 25.1% of those with suspicious preoperative FNAB findings would have required reoperation if intraoperative frozen section had not been performed (Table 4Go). The sensitivity, specificity, PPV, NPV, and accuracy of intraoperative frozen section in patients in this series with FNAB results of suspicious or follicular lesions were 83.9%, 100%, 100%, 94.9%, and 96.0%, respectively. These analytical findings indicate that frozen section is effective in determining the extent of operation for suspicious or follicular lesions, thereby decreasing discomfort and eliminating the cost for reoperation.

Some studies have reported enhanced sensitivity and specificity in detecting malignancy when FNAB and frozen section are combined.27,38,44,45 The studies have recommend using frozen section in each case. Conversely, others proposed that frozen section provides no additional information in thyroid surgery and have advocated eliminating frozen section.5,12–14,26 The role of FNAB and frozen section in thyroid nodule treatment is best characterized by assessing patients who have undergone both FNAB and frozen section (Table 4Go). Frozen section detected malignant lesions in 2.5% of benign FNABs, and only 50% of those with FN FNAB findings were diagnosed as malignant by frozen section (Table 4Go), thus indicating that frozen section is unnecessary for those with benign FNAB diagnoses. This study also determined that routine frozen section in all cases is not cost-effective. Therefore, we do not recommend frozen section for all cases, especially for those with benign FNAB findings. Conversely, frozen section detected malignant tumors in 21.1% of those with suspicious FNABs and in 88.2% of those with malignant FNABs. Furthermore, frozen section detected benign lesions in 11.8% of cases with malignant FNABs, thus decreasing the number of unnecessary total/near-total thyroidectomies. Performing frozen section in patients with suspicious or malignant diagnosis will not increase cost. Therefore, it is clear that frozen section has a significant effect on determining the extent of thyroidectomy in cases with suspicious and malignant FNAB lesions.

In conclusion, the data presented in this study confirm the efficacy of FNAB in selecting patients who require operation. However, its low specificity and accuracy do not permit adequate planning for surgical extent. Conversely, frozen section had a high specificity and resulted in a decreased number of reoperations. Routine application of frozen section is not necessary for benign FNAB results, because it contributes only slightly to the decision-making process and is not cost-effective. Frozen section, however, is cost-effective and specific in determining the extent of operation in patients with suspicious or malignant FNAB results.


   ACKNOWLEDGMENTS
 
The authors thank Chang Gung Memorial Hospital, Taoyuan, Taiwan, for partially supporting this research under Contract BMRP 072.

Received for publication May 10, 2006. Accepted for publication May 18, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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