ORIGINAL ARTICLE

Outcomes of incidentally discovered thyroid nodules referred to a high-volume head and neck surgeon
Teresa R. Kroeker, MD,* Gavin le Nobel, MD, Mazin Merdad, MD, Jeremy L. Freeman, MD
Department of Otolaryngology, Head and Neck Surgery, University of Toronto, Mount Sinai Hospital, Toronto, Ontario.

Accepted 22 January 2013 Published online 1 June 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.23273

ABSTRACT: Background. Incidental thyroid nodules are commonly

found by radiological studies done for other indications. The yearly incidence of thyroid cancer is increasing, in part because of detection of nonpalpable nodules on imaging performed for unrelated issues. Methods. All new patients referred to a high-volume thyroid surgeon for thyroid nodules were reviewed between February 2009 and January 2011. Data regarding patient demographics, risk factors, referring physician, radiologic findings, fine-needle aspiration (FNA) results, and management were reviewed.

Results. One hundred thirty-three of 729 patients (18.2%) had a thyroid nodule or nodules incidentally found on ultrasound, MRI, CT, nuclear imaging, or chest x-ray. Fifty-five patients (41.4%) were managed surgically, with 35 (63.6%) of those having thyroid cancer on final surgical pathology. Conclusion. Based on radiologic findings, risk factors, and FNA results, many incidental thyroid nodules can be observed. Incidental thyroid nodules should be evaluated in the same fashion as a palpable thyroid C 2013 Wiley Periodicals, Inc. Head Neck 36: 126129, 2014 nodule. V

KEY WORDS: incidental, thyroid, nodules, outcomes, management

INTRODUCTION
The yearly incidence of thyroid cancer is increasing, in part because of detection of nonpalpable nodules on ultrasound and cross-sectional imaging performed for unrelated issues. Incidental thyroid nodules are commonly found by radiological studies done for other indications. On ultrasound done for suspected parathyroid disease, 46% of patients were found to have incidental thyroid nodules.1 Similarly, thyroid incidentalomas have been identified in patients with an incidence of 16% for crosssectional imaging (CT and MRI),2,3 9% to 13% for carotid ultrasound,4,5 and 2% to 3% for positron emission tomography (PET) scans.68 The prevalence of incidental thyroid nodules on ultrasound in the general population ranges between 42% and 67%.9,10 Mazzaferri11 reported that patients greater than 40 years old have a 50% chance of having a thyroid nodule found on ultrasound as compared with a 5% chance of having a nodule found on physical examination. The Mayo clinic is well known for its study in 1955, in which they showed that in 821 autopsied patients with no history of thyroid disease, 50% were found to have a thyroid nodule.12 Schlumberger and Pacini13 also edited a report in 1999 that clinically occult thyroid nodules are found in 30% to 60% of autopsy

evaluations. The purposes of this study were (1) to determine what percent of all new referrals sent to a high-volume thyroid surgeon for a thyroid nodule were incidentally found thyroid nodules and (2) to determine how many of these incidental thyroid nodules were malignant.

MATERIALS AND METHODS

Approval was obtained from the Research Ethics Board at Mt. Sinai Hospital in Toronto, Ontario, to conduct a retrospective medical chart review in a single head and neck surgeons clinic. Charts of 729 new patients referred to a high-volume thyroid surgeon for a thyroid nodule were reviewed between February 2009 and January 2011. Data from 133 patients whose thyroid nodule/s was found incidentally were collected, including referring physician, patient demographics, risk factors, radiologic findings, fine-needle aspiration (FNA) results, management, and final surgical pathology.

RESULTS
One hundred thirty-three of 729 patients (18.2%) were found to have an incidental thyroid nodule. Of these 133 patients, 29% were men and 71% were women, with a mean age of 50 years old. Referral patterns for incidental thyroid nodules are depicted in Table 1. Most new referrals came from primary care physicians (52%), followed by endocrinologists (25%), otolaryngologists (18%), and other subspecialties (5%). Table 2 shows the radiologic imaging modality that led to the discovery of the incidental thyroid nodule, as well as the proportion from each modality that were malignant on final pathology. The vast majority were

*Corresponding author: T. R. Kroeker, 3705 Medical Parkway, Suite 250, Austin, TX 78705. E-mail: teresaruthk@gmail.com This work was presented at the 8th International Conference on Head and Neck Cancer, American Head and Neck Society, Toronto, Ontario, July 2012.

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TABLE 1. Referral pattern for incidental thyroid nodules.

No. of patients % of patients in study

TABLE 3. Reasons for radiologic imaging that led to discovery of incidental thyroid nodules.
No. of patients

Referring physician

Primary care physician Endocrinologist Otolaryngologist Other*

69 33 24 7

52 25 18 5

Reason

* Obstetrician-gynecologist, neurologist, neurosurgeon, cardiologist, or emergency department physician.

found on ultrasound (82%), followed by CT (9%), MRI (6%), and chest x-ray (3%). Indications for imaging include thyroid dysfunction (16%), neck discomfort (14%), lateral neck mass (11%), and globus and dysphagia (each 8%), as well as others depicted in Table 3. The average size of the incidental thyroid nodule was 19.7 mm, ranging from 2 to 56 mm. Of the 133 patients, 28 (21%) did not undergo FNA before or after consultation based on American Thyroid Association guidelines or patient preference. Sixty-five patients (49%) had an FNA of the dominant incidental thyroid nodule before consultation, and 55 patients (41%) underwent FNA after consultation, with FNA results depicted in Table 4. Ultrasound findings associated with respective FNA results are shown in Table 5. Fifty-four patients (41%) were managed surgically with extent of surgery and final surgical pathology shown in Table 6. Most patients (59%) underwent a total thyroidectomy alone, with an additional 22% who underwent a total thyroidectomy with a central neck dissection with or without a unilateral modified radical neck dissection or bilateral modified radical neck dissection for metastatic disease. Thirtyeight patients (29%) were found to have thyroid cancer on final surgical pathology, with 36 of those being papillary thyroid cancer, 1 medullary thyroid cancer, and 1 poorly differentiated carcinoma. The 1 patient with poorly differentiated carcinoma underwent a neck exploration with frozen section performed in the operating room. This patients preoperative FNA was insufficient after having been picked up incidentally on CT of the chest for a cough, which showed a large multinodular goiter with tracheal deviation. There was 1 patient with an FNA-diagnosed 6-mm papillary thyroid cancer who declined surgery and wished to be observed, and there were 2 patients with lesions suspicious for papillary thyroid cancer by FNA that did not follow-up with us after we recommended surgical treatment.

Thyroid dysfunction Neck discomfort Lateral neck mass Dysphagia Globus sensation Fatigue Shortness of breath Carotid ultrasound Hyperparathyroidism Hoarseness Weight change Screening Back pain Cough Tinnitus Trauma Visual changes/headache Night sweats Insomnia Hemoptysis

21 18 14 11 11 8 7 6 5 5 3 3 3 2 2 2 2 1 1 1

covered thyroid nodules vary, ranging from 8% to 29%. Papini et al14 reviewed 402 consecutive patients with nonpalpable thyroid nodules and found a malignancy rate of 8%, whereas Kang et al15 reviewed 1475 patients with nonpalpable nodules in Korea and found 29% to be malignant. In a review by Nam-Goong et al,16 12% of 267 patients with incidental thyroid nodules were found to be malignant. Jin et al17 reviewed 150 patients with incidental thyroid nodules and found 15% to be malignant. Liebeskind et al18 also looked at malignancy rates in incidentally found nodules versus nonincidental nodules and found that the malignancy rate was higher (17%) in the incidental group versus the nonincidental group (3%). Wilhelm et al19 looked at patients with incidental thyroid nodules with another primary malignancy and found 24% of them to be malignant. In our series of 133 incidentalomas, 29% were found to be malignant. The high malignancy rate in incidental thyroid nodules is likely because of several factors. A significant
TABLE 4. Biopsy results of patients with incidental thyroid nodules.
No. of patients

DISCUSSION
Palpable thyroid nodules have a reported malignancy rate of around 5%. Malignancy rates of incidentally disTABLE 2. Radiologic imaging modality that led to discovery of incidental thyroid nodules and proportion of malignancy on final pathology.
No. of patients % of patients in study % malignant

Biopsy classification

FNA diagnosis

Malignant Indeterminate

Imaging modality

Benign Ultrasound CT scan MRI Chest x-ray 109 13 8 4 82 9 6 3 28 38 13 0 Nondiagnostic

PTC MTC Suspicious for PTC Follicular neoplasm Hurthle cell neoplasm AUS/FLUS Colloid nodule/hyperplastic nodule/thyroiditis Insufficient

18 1 6 6 4 20 41 9

Abbreviations: FNA, fine-needle aspiration; PTC, papillary thyroid carcinoma; MTC, medullary thyroid carcinoma; AUS, atypia of undetermined significance; FLUS, follicular lesion of undetermined significance.

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contributor is likely a referral bias. Referring physicians may have chosen to not refer a patient with a subcentimeric simple thyroid cyst found on ultrasound. Most of our referring physicians were primary care physicians (52%) and endocrinologists (25%). Therefore, one of the weaknesses of this study is that our series of patients is not representative of the general population as many patients were likely excluded by the referring physician. We do not know how many patients were excluded in this manner. Another factor contributing to our high malignancy rate is that we included microcarcinomas in our proportion of malignancy, as did the previously mentioned studies. If we exclude the 13 patients with microcarcinoma, our incidentaloma malignancy rate would be 19%, as compared with 29%. We know that the prevalence of occult thyroid cancer in the United States ranges from 0.45% to 13%, with an estimated mean prevalence of 3.9% 6 4.1%.20,21 Our malignancy rate is reported in the same manner as historical literature on this topic, which includes nonoperative cases of incidental thyroid nodules. We understand that this percentage may not be entirely accurate, as there is no pathology report for the nonoperated patients, and there may be nondiagnosed cancers. If we were to only include surgically managed incidental thyroid nodules, our malignancy rate would be much higher at 70%. As previously mentioned, incidental thyroid nodules have been identified in 16% of cross-sectional imaging (CT and MRI),2,3 9% to 13% of carotid ultrasound scans,4,5 and 2% to 3% of PET scans.68 Shetty et al2 reviewed 230 patients with incidental thyroid nodules discovered on CT and found a 4% prevalence of malignancy. Yoon et al22 reviewed 123 patients with incidental thyroid nodules found on CT and found a 9.4% prevalence of malignancy. A slightly higher malignancy rate of 11% was reported by Jin et al17 in 84 patients found to have incidental thyroid nodules on CT. Only 13 of our patients had incidental thyroid nodules discovered on CT scan, and 5 of those (38%) were malignant. Most of the referrals in our series for an incidental thyroid nodule were found by ultrasound scan (82%), and 29% of those were found to be malignant. Although we did not have any incidental thyroid nodules identified by PET scan, studies have shown a much higher rate of malignancy in these nodules, ranging between 14% and 50%.68,17
TABLE 5. Fine-needle aspiration results and associated ultrasound findings.
Stippled calcifications (%)

TABLE 6. Surgical management of 54 patients with incidental thyroid nodules and final surgical pathology.
No. of patients % of patients

Variable

Type

Surgery

Pathology

TT TT CND TT CND UND TT CND BND ST Neck exploration PTC Papillary microcarcinoma MTC Dedifferentiated Benign

32 4 6 2 9 1 23 13 1 1 16

59 7 11 4 17 2 42 24 2 2 30

Abbreviations: TT, total thyroidectomy; CND, central neck dissection; UND, unilateral modified radical neck dissection; BND, bilateral modified radical neck dissection; ST, subtotal thyroidectomy; PTC, papillary thyroid carcinoma; MTC, medullary thyroid carcinoma.

Incidental thyroid nodules should be evaluated in the same fashion as a palpable thyroid nodule, according to the American Thyroid Association guidelines. A thorough history including age, sex, thyroid disease history, history of radiation exposure to the head or neck, and family history of thyroid cancer or endocrine malignancies must be obtained. Management of thyroid nodules should be more aggressive if the patient has a family history of thyroid cancer or a history of head and neck radiation as a child. There is no evidence that incidentally discovered thyroid nodules are at increased risk for malignancy, but a higher percentage will be found to be malignant secondary to a significant referral bias. We have shown that with the increased number of thyroid nodules being detected incidentally, more and more endocrinologists and surgeons will be inundated with these referrals. Kang et al15 looked at 1475 patients who visited Samsung Medical Center in Seoul, Korea, and the prevalence of thyroid incidentalomas was 13.4%. In our series, 18% of all of our new referrals for thyroid nodules over a 2-year period were incidentally discovered. Because of the possibility of poorly documented histories in the reviewed patient medical charts, this number may actually be higher in reality. Of these 133 patients, 41% were managed surgically, with 29% of them having thyroid cancer on final surgical pathology. Based on radiologic findings, risk factors, and FNA results, many of these can be observed and followed with serial ultrasounds.

FNA diagnosis

Isolated nodule (%)

Average size, mm

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PTC MTC Suspicious for PTC Follicular neoplasm Hurthle cell neoplasm AUS/FLUS Benign Nondiagnostic

7/18 (39) 1/1 (100) 2/6 (33) 3/6 (50) 1/4 (25) 7/20 (35) 12/41 (29) 5/9 (56)

11/18 (61) None 3/6 (50) None 1/4 (25) 5/20 (25) 10/41 (24) 4/9 (44)

19 17 19 17 17 25 22 19

Abbreviations: FNA, fine-needle aspiration; PTC, papillary thyroid carcinoma; MTC, medullary thyroid carcinoma; AUS, atypia of undetermined significance; FLUS, follicular lesion of undetermined significance.

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