Neuroradiology/Head and Neck Imaging Original Research

Neuroradiology/Head and Neck Imaging Original Research Hobbs et al. FNA of Thyroid Nodules Neuroradiology/Head and Neck Imaging Original Research Hasan A. Hobbs 1 Manisha Bahl 1 Rendon C. Nelson 1,2 James D. Eastwood 1 Ramon M. Esclamado 2,3 Jenny K. Hoang 1,4 Hobbs HA, Bahl M, Nelson RC, Eastwood JD, Esclamado RM, Hoang JK Keywords: Society of Radiologists in Ultrasound, thyroid, thyroid nodule DOI:10.2214/AJR.13.11219 Received May 11, 2013; accepted after revision June 15, 2013. 1 Department of Radiology, Division of Neuroradiology, Duke University Medical Center, DUMC Box 3808, Durham, NC 27710. Address correspondence to J. K. Hoang (jennykh@gmail.com). 2 Department of Radiology, Division of Abdominal Imaging, Duke University Medical Center, Durham, NC. 3 Department of Surgery, Division of Otolaryngology- Head and Neck Surgery, Duke University Medical Center, Durham, NC. 4 Department of Radiation Oncology, Duke University Medical Center, Durham, NC. This article is available for credit. AJR 2014; 202:602 607 0361 803X/14/2023 602 American Roentgen Ray Society Applying the Society of Radiologists in Ultrasound Recommendations for Fine-Needle Aspiration of Thyroid Nodules: Effect on Workup and Malignancy Detection OBJECTIVE. The Society of Radiologists in Ultrasound (SRU) recommendations on thyroid nodules are intended to diagnose thyroid cancers that have reached clinical significance, while avoiding unnecessary tests and surgery in patients with benign nodules. The aim of our study was to determine the proportion of thyroid nodules undergoing ultrasoundguided fine-needle aspiration (FNA) that do not meet SRU recommendations. MATERIALS AND METHODS. This study is a retrospective study of 400 consecutive ultrasound-guided thyroid FNA encounters from July 2010 through June 2011. An encounter was defined as presentation to the department of radiology on a given date for FNA of one or more thyroid nodules. The criteria for performing biopsy of a nodule were determined by the referring clinicians. Nodules were categorized on the basis of sonographic findings as meeting SRU recommendations for biopsy, which we refer to as SRU-positive, or not, which we refer to as SRU-negative. Patients without a definitive pathology diagnosis of Bethesda class benign or malignant nodules were excluded. The characteristics of malignancies were compared for SRU-positive and SRU-negative encounters. RESULTS. The final study group consisted of 360 biopsy encounters for 350 patients and 29 malignancies (8%). Of the 360 biopsy encounters, 86 (24%) were SRU-negative encounters. Malignancy rates in SRU-positive and SRU-negative encounters were 9% (24/274) and 6% (5/86), respectively, and were not significantly different (p = 0.5). Eighteen malignancies (75%) in the SRU-positive group were localized, whereas the others had nodal metastases (4/24) or distant metastases (2/24). SRU-positive encounters included medullary carcinoma, anaplastic carcinoma, and melanoma metastasis in addition to papillary carcinoma. All SRUnegative malignancies were localized papillary carcinomas. CONCLUSION. One in four thyroid biopsy encounters at our institution did not meet SRU recommendations for biopsy. The application of SRU recommendations reduces the number of benign nodules that undergo workup. Potentially missed malignancies in SRUnegative nodules are less aggressive by histologic type and stage compared with SRU-positive malignancies. T he Society of Radiologists in Ultrasound (SRU) provided sonographic criteria for the management of thyroid nodules in an article published in 2005 [1]. The SRU is an American society, and the criteria were developed by a panel of experts from several medical disciplines, including radiology, endocrinology, cytopathology, and surgery. These guidelines attempted to define recommendations for nodules that should and should not undergo ultrasound-guided fineneedle aspiration (FNA). The SRU recommendations assert that FNA is appropriate for nodules that are 10 mm or larger and have microcalcifications, nodules that are 15 mm or larger and are solid or have coarse calcifications, nodules that are 20 mm or larger and are mixed solid and cystic, and nodules with substantial growth since the prior ultrasound study. Despite the guidelines, the number of thyroid nodules undergoing ultrasound-guided FNA has continued to increase because more thyroid nodules undergo biopsy as a result of fear of missing a malignancy [2]. Many thyroid nodules undergoing sonographic workup are small incidental thyroid nodules detected on imaging. Although early diagnosis may be favorable in some malignancies, this may not be the case for thyroid cancer because the majority of the malignancies detected are small papillary carcinomas [3]. 602 AJR:202, March 2014

FNA of Thyroid Nodules TABLE 1: Study Subjects and Nodules Many experts believe that these small thyroid cancers represent pseudodisease and that most patients die with thyroid cancer rather than of thyroid cancer [1, 3]. Thus, an ideal approach to selecting which incidental thyroid nodules should undergo workup would not be to diagnose all cancers but, rather, to diagnose cancers that have reached clinical significance, while avoiding unnecessary tests and surgery in patients with benign nodules [1]. This statement is emphasized by the SRU recommendations. Although the specific intent of the SRU recommendations was to reduce the unnecessary workup of thyroid nodules, there were concerns that the recommendations could in fact lead to an increase in the number of thyroid FNAs and subsequent thyroid surgeries [1]. To date, the effect of the guidelines on thyroid FNA volume and malignancy rate and the acceptance of the guidelines in practice have not been evaluated. The aim of this study was to determine the proportion and type of thyroid nodules undergoing ultrasound-guided FNA at our institution that do not meet the SRU recommendations, which we refer to as SRU-negative. Our hypothesis was that many thyroid nodules undergoing FNA do not meet SRU recommendations and that SRU-negative malignancies are uncommon and are less aggressive. Materials and Methods Subjects and Pathologic Categorization This study was approved by our institutional review board and was compliant with the HIPAA. We retrospectively reviewed the records of 400 consecutive ultrasound-guided thyroid FNA encounters through the department of radiology during a 12-month period from July 2010 through June 2011. An encounter was defined as presentation to the department of radiology on a given date for FNA of one or more thyroid nodules. The criteria for selecting which nodule or nodules to biopsy were determined by the referring endocrinologists and endocrine surgeons, not the radiologist. In our institution the most common practice for diagnostic ultrasound is to report thyroid nodules 10 mm or larger in the impression section of the ultrasound report without adding a statement to recommend biopsy of the nodule unless there are highly suspicious features such as microcalcifications or hypoechogenicity. The medical records of all included patients were reviewed for the age and sex of the patient, pathologic diagnosis, and management. The pathologic diagnosis was defined by a surgical pathologic result if available (n = 87 patients) and an FNA cytopathologic result (n = 263 patients) if the patient did not undergo surgery. At our institution, FNA cytopathology results are characterized by the Bethesda System for Reporting Thyroid Cytopathology [4]. The Bethesda class categories include the following: class I, nondiagnostic or unsatisfactory; II, benign; III, atypia of undetermined significance or a follicular lesion of undetermined significance; IV, a follicular neoplasm or suspicious for a follicular neoplasm; V, suspicious for malignancy; and VI, malignant. Nodules with FNA cytopathologic results revealing Bethesda class I, III, IV, or V are not regarded as definitive results, and the Bethesda System [4] recommends repeat biopsy for classes I and III and diagnostic surgery for classes IV, V, and VI. A class II result is considered benign, and patients with a class II result do not undergo further biopsy or surgery. In this study, patients with a Bethesda class I, III, IV, or V result who did not undergo repeat Total Benign Malignant Characteristic No. % No. % No. % No. of encounters 360 331 29 No. of patients 350 321 29 Sex Male 60 17 51 16 9 31 Female 290 83 270 84 20 69 Age (y) Mean (SD) 55 (14) 55 (15) 54 (14) No. (%) of encounters by patient age 0 19 y 4 1 4 1 0 0 20 34 y 32 9 28 8 4 14 35 49 y 74 21 69 21 5 17 50 64 y 156 43 145 44 11 38 65 y 94 26 85 26 9 31 Size of largest nodule for encounter (mm) Mean (SD) 26 (14) 26 (14) 28 (16) No. (%) of encounters by size of largest nodule 5 9 mm 13 4 13 4 0 0 10 14 mm 61 17 55 17 6 21 15 19 mm 84 23 79 24 5 17 20 mm 202 56 184 55 18 62 Note An encounter was defined as presentation to the department of radiology on a given date for fine-needle aspiration of one or more thyroid nodules. AJR:202, March 2014 603

Hobbs et al. Thyroid FNAs performed during study period (n = 400) Benign (n = 250) SRU-positive (n = 274) FNAs included: Bethesda class II or VI cytopathologic result or final surgical pathology (n = 360) Malignant (n = 24) FNA or surgery were excluded from the study group. All malignancies (Bethesda class VI) were further followed for the stage of disease, treatment response, and overall survival. Benign (n = 81) SRU-negative (n = 86) Malignant (n = 5) Application of SRU Recommendations Diagnostic ultrasound (iu22 unit, Philips Healthcare) images of the thyroid nodules were obtained before the biopsy using a 12- MHz transducer. Thyroid nodules were measured on the ultrasound unit by the technologist or radiologist at the time of imaging and were documented in the examination report. These sizes were used, and the nodule was not measured retrospectively. A board-certified radiologist (7 years of experience) reviewed the ultrasound images on a PACS workstation for findings according to the SRU recommendations. SRU recommendations were met if the biopsied nodule had any of the following characteristics: size of 10 mm or larger with microcalcifications, size of 15 mm or larger with solid composition or coarse calcifications, size of 20 mm or larger with mixed solid-cystic composition, or substantial growth since the prior ultrasound. Because the SRU consensus statement does not explicitly define the requirements for substantial growth, a nodule was considered to show substantial growth if interval growth was the reason for the FNA and the nodule possessed no other criteria meeting SRU recommendations. Past ultrasound studies preceding the last diagnostic thyroid ultrasound were not reviewed specifically for substantial change. Biopsy encounters were categorized on the basis of the sonographic findings as meeting the SRU recommendations for biopsy, which we refer to as SRU-positive, or not. We measured potential reduction of workup by the number of patient encounters rather than individual nodules because the greatest cost saving is in preventing any FNA rather than preventing FNA of a second or third thyroid nodule. In patients who had more than one nodule biopsied during an encounter (n = 120), the encounter was categorized as SRUpositive if any nodule met the SRU recommendations or as SRU-negative if none of the nodules met the recommendations. SRU-negative encounters comprise the subgroup of patients for whom workup with FNA could have been avoided if the SRU recommendations had been applied at the time of biopsy. FNAs excluded: Bethesda class I, III, IV, or V cytopathologic result without repeat FNA or surgery (n = 40) SRU-positive (n = 30) 12 Bethesda class I 15 Bethesda class III 2 Bethesda class IV 1 Bethesda class V SRU-negative (n = 10) 7 Bethesda class I 3 Bethesda class III Fig. 1 Flowchart shows study cohort. Fine-needle aspiration (FNA) biopsy encounters were categorized on basis of sonographic findings as having met Society for Radiologists in Ultrasound (SRU) recommendations for biopsy, which we refer to as SRU-positive, or as not, which we refer to as SRU-negative. FNA cytopathologic results are characterized by Bethesda System for Reporting Thyroid Cytopathology [4]. Bethesda class categories include class I, nondiagnostic or unsatisfactory; II, benign; III, atypia of undetermined significance or follicular lesion of undetermined significance; IV, follicular neoplasm or suspicious for follicular neoplasm; V, suspicious for malignancy; and VI, malignant. Statistical Analysis Nodules biopsied in the SRU-positive and SRU-negative encounters were compared for size, malignancy rate, and characteristics of the malignancies (size, histologic diagnosis, and stage). The proportion of nodules not meeting the SRU recommendations was calculated as follows: (SRU-negative nodules / total nodules) 100. The malignancy rates in the SRU-positive and SRU-negative groups were compared with the Fisher exact test. The sensitivity and specificity of the SRU recommendations for thyroid malignancy were also calculated. Results Subjects and Pathology Four hundred biopsy encounters were performed for 390 patients during the study period. Forty patients were excluded because FNA cytopathologic results revealed Bethesda class I, III, IV, or V without repeat FNA or surgery for definitive pathology results. The final study group consisted of 360 biopsy encounters in 350 patients (290 female, 60 male; mean age, 604 AJR:202, March 2014

FNA of Thyroid Nodules TABLE 2: Characterization of Biopsy Encounters According to Whether Society of Radiologists in Ultrasound (SRU) Recommendations for Biopsy Were Met ( SRU-Positive ) or Not ( SRU-Negative ) Biopsy Encounters No. (%) of Encounters by SRU Criteria SRU Criteria No. % 10 mm With Microcalcifications 15 mm Solid Composition or With Coarse Calcifications 20 mm Mixed Solid and Cystic Substantial Growth Since Last Ultrasound SRU-positive 274 Benign 250 91 34 (89) 174 (91) 40 (95) 2 (100) Malignant 24 9 4 (11) 18 (9) 2 (5) SRU-negative 86 Benign 81 94 Malignant 5 6 Note An encounter was defined as presentation to the department of radiology on a given date for fine-needle aspiration of one or more thyroid nodules. 55 years; age range, 7 91 years) (Table 1 and Fig. 1). In all patients, diagnostic ultrasound images of the thyroid nodule or nodules were obtained during the procedure. Almost all patients had undergone diagnostic ultrasound at a date before the ultrasound-guided FNA procedure. Sixty patients had incidental nodules seen initially on CT, MRI, or PET/CT. One hundred twenty patients (34%) underwent biopsy of more than one nodule, and a total of 507 nodules were biopsied. The mean nodule size was 26 ± 14 (SD) mm, and only 13 of 507 (2.5%) nodules were less than 10 mm in diameter. There were 29 malignancies in 360 encounters (8% malignancy prevalence), all of which were confirmed on final surgical pathology. The patients with malignancy had a mean age of 54 years (age range, 20 70 years), and 20 of 29 (69%) were female. SRU Recommendations and Malignancy There were 397 SRU-positive and 110 SRU-negative nodules. In the 360 biopsy encounters, 274 had at least one SRU-positive nodule and 86 were SRU-negative (Table 2). If SRU recommendations had been applied before biopsy, 86 of 360 (24%) encounters would not have resulted in biopsy and 110 of 507 (22%) nodules would have not undergone a biopsy. In the SRU-positive group, 250 (91%) had a benign pathologic result and 24 (9%) had a malignant pathologic result. In the SRU-negative group, 81 (94%) had a benign pathologic result and five (6%) had a malignant pathologic result. There was no significant difference in the malignancy rates of the two groups (p = 0.50). The SRU-positive thyroid malignancies included 17 localized papillary carcinomas, four papillary carcinomas with nodal metastases, one localized medullary carcinoma, one anaplastic carcinoma with distant metastases, and one melanoma metastasis (Table 3). There was one tumor-related death during the study period: The diagnosis in that case was anaplastic thyroid carcinoma with metastases. All SRU-negative malignancies were localized papillary carcinomas that were 14 mm or smaller (Table 3). If the SRU recommendations had been applied before the biopsy, these five localized papillary thyroid carcinomas would not have been biopsied. Thus, applying the SRU recommendations would have resulted in a false-negative rate of 17% (5 missed malignancies / 29 total malignancies). The sensitivity and specificity of the SRU recommendations for thyroid malignancy in our cohort were 83% and 25%, respectively. Of the 40 biopsy encounters that were excluded because of no definitive pathologic diagnosis, 30 were SRU-positive encounters and were in the following Bethesda class: 12, class I; 15, class III; two, class IV; and one, class V. Ten encounters were SRU-negative: seven were class I and three were class III. Discussion The SRU recommendations were developed by an expert group of radiologists to assist physicians in deciding which nodules seen on ultrasound should undergo FNA. One of the concerns of the SRU was the unknown effect of the guidelines on the workup rate of thyroid nodules and the possibility that they could increase, rather than decrease, FNA and subsequent surgery. This study shows that using the SRU criteria for ordering ultrasound-guided FNA at our institution could have eliminated one in four biopsy encounters compared with current practice at our institution. The malignancies diagnosed in nodules that did not meet SRU criteria had a less aggressive histologic diagnosis than the SRU-positive malignancies. The SRU recommendations have been studied by Ahn et al. [5], who applied the criteria to nodules undergoing ultrasound-guided biopsy in their institution in South Korea. In their study, nodules smaller than 10 mm were also biopsied, which is not standard practice for nodules in low-risk patients in the United States without other suspicious sonographic findings [1, 6]. In our study, only 13 nodules were smaller than 10 mm. In their study [5], Ahn et al. performed an analysis of a subset of nodules 10 mm or larger and found that 40% of nodules did not meet SRU recommendations (396 SRU-negative nodules / 996 total nodules). This proportion of SRU-negative encounters is much greater than in our study (24%) and likely reflects the differences in biopsy selection between our institutions. The performance of the SRU recommendations reported as sensitivity and specificity for malignancy also differed between our studies: Ahn et al. found sensitivity and specificity to be 72% and 42%, respectively, whereas we found a higher sensitivity of 83% but a lower specificity of 25%. Sensitivity and specificity are dependent on the prevalence of disease; the prevalence of malignancy in our study group was 8%, compared with 16% in the study by Ahn and colleagues. The malignancy rate in our study is more consistent with those of other studies, and a recent meta-analysis of more than 25,000 FNA biopsies reported 5.4% of nodules were classified as malignant (Bethesda class VI) and 8.1% were classified as suspicious for malignancy (Bethesda class V) or malignant (Bethesda class VI) [7]. Multiple guidelines exist for the evaluation and workup of thyroid nodules based on sonographic criteria. In addition to the SRU guidelines, other major guidelines are from the National Comprehensive Cancer Network (NCCN), American Association of Clinical Endocrinologists (AACE), and American Thyroid Association (ATA) [6, 8, 9]. These guidelines may be the guidelines that some of our endocrinologists and surgeons use in recommending biopsy. The NCCN guidelines are most similar to the SRU guidelines in that the size cutoff for solid nodules without suspicious features is 15 AJR:202, March 2014 605

Hobbs et al. TABLE 3: Categorization of Biopsies, Pathologic Results, and Treatments for Encounters That Met Society of Radiologists in Ultrasound (SRU) Recommendations for Biopsy ( SRU-Positive ) and Encounters That Did Not ( SRU-Negative ) Characteristic SRU-Positive SRU-Negative Total No. of biopsy encounters 274 86 360 Size of nodule (mm) Mean (SD) 30 (16) 13 (3) Pathologic result, no. (%) of nodules Benign 250 (91) 81 (94) 331 Malignant 24 (9) 5 (6) 29 Stage of thyroid malignancy, no. (%) of nodules Localized 18 (75) 5 (100) 23 Regional 4 (17) 0 4 Metastatic 1 (4) 0 1 Metastasis to thyroid gland 1 (4) 0 1 Additional procedures in benign nodules, no. (%) of nodules Surgery for benign disease 58 (23) 5 (6) 63 Follow-up imaging 68 (27) 33 (40) 101 Note An encounter was defined as presentation to the department of radiology on a given date for fine-needle aspiration of one or more thyroid nodules. mm. Both the AACE and ATA recommend biopsy for solid nodules larger than 10 mm. In addition, the AACE recommends biopsy of any size nodule with one or more suspicious sonographic findings [8]. Overall, the larger size cutoff of the SRU and NCCN recommendations would result in higher specificity (workup of fewer benign cases) than the AACE and ATA guidelines for our cohort of patients. As seen from our results, the specificity for the SRU recommendations is already very low (25%). The cost of higher specificity for malignancy is a potentially higher false-negative rate and more missed malignancies. The falsenegative rate in our study was 17% for the SRU recommendations, but all the SRU-negative malignancies were smaller than 15 mm and were localized to the thyroid. Cancers of this size, histologic type, and stage have excellent survival of greater than 99%, and several experts believe that many of these patients will die with rather than of thyroid cancer [6, 10]. A contentious question for future research is whether treatment of small localized papillary cancers improves survival [11]. Postmortem studies show that a certain number of small thyroid cancers will remain indolent in a patient s life, with up to 36% of patients having undiagnosed thyroid cancer at death [12]. If the small SRU-negative cancers were undiagnosed, untreated, and progressed to a larger size, the survival could still be excellent. Ito et al. [13] followed 340 papillary microcarcinomas that were selected to not receive treatment: After 10 years, there were new nodal metastases in 3% of cases and no cancer deaths [13]. For these reasons, the SRU recommendations specifically aim to diagnose cancers that have reached clinical significance, while avoiding unnecessary tests and surgery in patients with benign nodules [1]. Our study shows that SRU recommendations achieve this goal by missing only localized papillary carcinomas while reducing workup by one quarter. There are several limitations to this study. First, this study is a retrospective study at one academic center conducted over a limited period of 12 months. Our results may not be generalizable to different practice types and referral patterns. Second, FNAs performed in the department of radiology do not include all thyroid FNAs at our institution. FNAs of thyroid nodules are also performed using ultrasound guidance by surgeons, endocrinologists, and pathologists, and these FNAs were not included. The nodules biopsied by clinicians and pathologists might have a higher proportion of SRU-negative nodules due to more liberal biopsy practices because of convenience of biopsy in a clinic, or the opposite could occur because clinic biopsies may be performed on larger nodules that are less technically challenging to biopsy. Third, ultrasound studies were reviewed by a single reader, and additional readers could yield slightly different results in the performance of SRU recommendations because of interreader variability. We also did not review all past ultrasound studies for the criterion of substantial growth because what constitutes substantial growth has not been specifically defined by the SRU. Finally, we applied the criteria based on the imaging findings and clinical information available. There could be other clinical information that was not available in the medical records that put the patients at higher risk of malignancy to warrant a biopsy. In conclusion, the SRU recommendations achieve the goal of diagnosing cancers that have reached clinical significance, while avoiding unnecessary tests and surgery in patients with benign nodules [1]. Using SRU recommendations can reduce workup of one in four thyroid biopsy encounters compared with current practice without strict guidelines. Potentially missed malignancies in SRU-negative nodules are less aggressive by histologic type, size, and stage compared with SRU-positive malignancies. References 1. Frates MC, Benson CB, Charboneau JW, et al.; Society of Radiologists in Ultrasound. Management of thyroid nodules detected at US: Society of Radiologists in Ultrasound consensus conference statement. Radiology 2005; 237:794 800 2. Coorough N, Hudak K, Buehler D, Selvaggi S, Sippel R, Chen H. Fine needle aspiration of the thyroid: a contemporary experience of 3981 cases. J Surg Res 2011; 170:48 51 3. Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973 2002. JAMA 2006; 295:2164 2167 606 AJR:202, March 2014

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