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Importance of surgeon-performed ultrasound in the preoperative nodal assessment of patients with potential thyroid malignancy
ARTICLE IN PRESS Surgery ■■ (2017) ■■–■■
Contents lists available at ScienceDirect
Surgery j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y m s y
American Association of Endocrine Surgeons
Importance of surgeon-performed ultrasound in the preoperative nodal assessment of patients with potential thyroid malignancy Rosebel Monteiro, MD a, Amy Han, BS b, Muhammad Etiwy, MD b, Andrew Swearingen, MD b, Vikram Krishnamurthy, MD b, Judy Jin, MD b, Joyce J. Shin, MD b, Eren Berber, MD b, and Allan E. Siperstein, MD b,* a b
Department of Endocrine Surgery, The Cleveland Clinic Foundation, Cleveland, OH Case Western Reserve School of Medicine, Cleveland, OH
A R T I C L E
I N F O
Article history: Accepted 6 October 2017
Introduction. A comprehensive cervical ultrasound evaluation is essential in the operative planning of patients with thyroid disease. Reliance on radiographic reports alone may result in incomplete operative management as pathologic lymph nodes are often not palpable and evaluation of the lateral neck is not routine. This study examined the role of surgeon-performed ultrasound in the evaluation of patients who underwent lateral neck dissection for thyroid cancer. Methods. We conducted a retrospective review of a prospectively maintained database of patients who underwent therapeutic lymph node dissection for thyroid cancer between 2001 and 2016 at our tertiary referral center. All patients had surgeon-performed ultrasound preoperatively by 1 of 7 endocrine surgeons. These findings were compared with prereferral imaging studies to determine the value of surgeonperformed ultrasound to their overall treatment. Results. Of 92 patients who underwent thyroidectomy with lateral neck dissection, 97% had prereferral imaging of the neck (ultrasonography, computed tomography, positron emission tomography). Of these patients, nodal disease was suggested by computed tomography scanning in 70.8% and by ultrasonography in 54%. Of all patients, 45% had positive lateral neck nodes detected only on surgeon-performed ultrasound despite prior neck imaging. Nodal disease was identified in 50% of patients with only 1 study and 50% of patients with greater than 1 study before surgeon-performed ultrasound. Of patients with nodes detected by surgeon-performed ultrasound, only 67% had a prereferral diagnosis of thyroid cancer. Conclusions. Our data demonstrate that reliance on standard preoperative imaging alone would have led to an incorrect initial operation in 45% of our patients. Awareness of the limitations of prereferral imaging is important for surgeons treating patients with thyroid and parathyroid disease. Surgeonperformed ultrasound is a useful tool in the diagnosis and accurate staging of patients. © 2017 Elsevier Inc. All rights reserved.
Introduction Ultrasonography (US) is a noninvasive, low-cost imaging modality that has had widespread utility in the detection, diagnosis, and treatment of patients with thyroid and parathyroid disease. The value of surgeon-performed ultrasound (SUS) has broadened to include the characterization of benign and malignant thyroid disease, evaluation of the lymph nodes, performance of fine-needle aspiration (FNA) of the lesion or the lymph node, intraoperative localization of disease, as well as postoperative surveillance of recurrence.1,2 High-resolution US has previously been shown to
Presented at the 38th Annual Meeting of the American Association of Endocrine Surgeons. * Reprint requests: Allan E Siperstein, MD, Case Western Reserve School of Medicine, Cleveland, OH. E-mail: [email protected].
modify the surgical approach in up to 40% of patients with thyroid cancer.3 Cervical lymph node metastasis occurs in up to 30% of patients with papillary thyroid carcinoma,4 while medullary thyroid carcinoma demonstrates early nodal metastases in up to 50% of patients.5 Earlier studies have also demonstrated that SUS of the lateral neck is reliable with a high sensitivity and negative predictive value.6 Sonographically detectable nodal metastases in the lateral compartment have been shown to be indicators of local recurrence, as well as poorer relapse-free survival in patients with papillary thyroid cancer.7,8 Furthermore, the 2015 American Thyroid Association (ATA) guidelines recommend that US evaluation of the anterior cervical lymph node compartments (central and lateral) be performed when thyroid nodules are detected.9 Thus, in patients presenting with documented or potential thyroid cancer, accurate preoperative staging, particularly of the lateral neck, is essential for the management of all identifiable disease with a single operation. Additionally, SUS has the potential to decrease the number of costly and time-consuming appointments for the patient and reduce
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Please cite this article in press as: Monteiro Rosebel, et al., Importance of surgeon-performed ultrasound in the preoperative nodal assessment of patients with potential thyroid malignancy, Surgery (2017), doi: 10.1016/j.surg.2017.10.005
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the number of expensive and invasive studies before definitive surgical treatment. Thus, surgeons should work toward a thorough preoperative staging so that the appropriate extent of surgery is performed at the initial operation. At our institution, all patients referred for thyroid or parathyroid disease routinely undergo SUS that includes a complete examination of the lymph nodes in the central (level VI) and lateral neck (levels II–V) regardless of the initial reason for referral or the presenting diagnosis. Sonographic features that should arouse suspicion of nodal metastases include round shape, increased size, irregular margins, calcifications, cystic components, peripheral vascularity, replaced fatty hilum, and heterogeneous echo texture.10,11 Our clinical observation is that in many patients, especially in patients with thyroid cancer, prereferral imaging often lacked details about structural neck nodal disease. Thus, reliance on prereferral imaging alone may result in incomplete initial preoperative staging and operative management with the potential need for a reoperation. In terms of preoperative surveillance, earlier studies have discussed the importance of preoperative cervical US and its accuracy in identifying nodal disease.12,13 It has been previously reported that central neck lymph nodes may be missed because of shadowing from tumors. However, at the time of index thyroidectomy, these central nodes are easily discovered as they are in the field of dissection. In contrast, the lateral compartment nodes are not routinely explored and are not in the operative field. Thus, accurate staging of the lateral neck is essential for planning the appropriate initial operation, as detecting lateral neck disease can address all identifiable disease in a single operation and decrease the potential for a re-operation. Earlier studies have not evaluated patients who are referred to endocrine surgeons with nodular thyroid disease or thyroid cancer with incomplete staging of the lateral neck on prereferral imaging. The purpose of this study is to systematically evaluate patients who underwent total thyroidectomy with therapeutic lateral neck dissection as the initial operation to assess the value of SUS to their overall treatment. Methods This was an institutional research board−approved retrospective analysis of patients from a prospectively maintained database. This database was queried for patients who underwent therapeutic lymph node dissection for thyroid cancer at the Cleveland Clinic from January 1, 2001, to October 31, 2016. Before surgical referral, no imaging studies are routinely ordered by our surgeons. The prereferral imaging studies in our study were generally ordered by the referring physician (endocrinologist, primary care provider, etc); whereas all patients underwent SUS preoperatively by 1 of 7 endocrine surgeons. When SUS detects lateral neck cervical lymph nodes that are sonographically suspicious for thyroid cancer, FNA of the abnormal lymph nodes is performed for cytology and washout for thyroglobulin measurement routinely in all cases.9,14 Therapeutic central (level VI and VII) or lateral neck dissection (levels II–IV [upper, middle, and lower jugular nodes] and posterior triangle nodes [level V]) is then performed after FNA detection of malignancy or via elevated nodal thyroglobulin levels (normal <1 ng/mL). Our definition of lymph node dissections aligns with the 2012 ATA consensus statement.15 Although it is ideal to suspect central neck disease preoperatively, it is our practice to forgo performing FNA of suspicious central neck lymph nodes preoperatively because they are routinely sampled intraoperatively in patients with papillary thyroid cancer. A therapeutic central neck dissection is subsequently performed when and intraoperative frozen section reveals the presence of nodal metastases. In patients who are referred with a diagnosis of papillary thyroid cancer with no sonographically identifiable lateral neck disease, the lateral compartments are not explored.
We examined a group of patients who underwent total thyroidectomy with lateral neck dissection to determine the impact of SUS in patients who may have undergone an inadequate resection as a result of unassessed lateral neck disease. For these patients, findings of SUS were compared with prereferral imaging (group 1). Additionally, to assess the quality of our nodal surveillance, we studied patients who underwent initial surgery at our institution and were found to have lateral neck nodal disease at their 6-month postoperative oncologic follow-up visit, suggesting that this was missed at initial evaluation (group 2). We made the presumption that this was missed disease rather than interval progression of aggressive or evolving disease in order to assess the quality of our nodal surveillance. A 6-month period was chosen as this is the typical time frame for the initial post-operative longitudinal tumor surveillance after potential adjuvant radioactive iodine therapy. This time frame allows for adequate thyroid-stimulating hormone (TSH) suppression and monitoring of thyroglobulin levels and facilitates performance of high-quality US after postoperative changes have settled. Demographic and clinical data, biochemical and prereferral imaging, FNA results, extent of operation performed, and pathology from institutional review board–approved databases and patients’ records were retrospectively reviewed. Results This was a series of 92 patients who underwent total thyroidectomy and lateral neck dissection at our institution (group 1). Of these patients, 92% had papillary thyroid cancer and 8% had medullary thyroid cancer. Basic demographic data and operative characteristics including gender, age, BMI, and number and size of malignant nodes on final pathology are summarized in the Table. In all patients who eventually underwent total thyroidectomy with lateral neck lymph node dissection, 45% had disease initially detected on SUS (Fig 1). In 55% of patients, nodal disease was detected before the surgeon’s evaluation. In these patients with nodal disease detected before surgical evaluation, 61% had disease detected on US, 29% on CT, and 10% on magnetic resonance imaging (MRI). Among these patients with nodal disease detected on imaging studies before referral, only 22% of patients had lymph node FNA performed before surgical referral. The remaining 78% of patients had nodes reported on prereferral imaging, but FNA was not performed. The presence of lymph nodes was commonly mentioned on CT scan reports; however, the presence of these nodes did not necessarily indicate metastatic disease as no biopsy-proven diagnosis had occurred. SUS was utilized in these cases to confirm a tissue diagnosis and to accurately stage the patient. Before referral to a surgeon, 97% of patients (89/92) underwent at least one prereferral imaging study. Eighty-nine patients underwent a total of 124 studies before referral as some patients had more than 1 imaging study (Fig 2). Seventy-four percent of the patients underwent a prereferral US with 34% of patients that underwent an isolated US study, whereas 35% had a concurrent CT scan and 5% had a concurrent MRI/PET scan. Of the remaining patients, 19% underwent CT scan alone, and 4% underwent a PET/MRI scan
Table Patient demographics Age (average in years) Body mass index (average) Papillary thyroid carcinoma Medullary thyroid carcinoma Number of lateral nymph node resected Number of malignant lymph node on pathology Size of largest malignant lymph node (average)
43 ± 16.5 (11–75) 28.6 ± 6.9 (17–55) 91.30% 8.70% 19.7 ± 13.3 9.9 ± 7.7 cm 2.3 ± 1.0 cm (0.1–5.3 cm)
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Fig 1. Distribution of patients by mode of initial detection of lateral neck nodal disease. In all patients who eventually under TT+ LND, 45% of patients had disease detected initially on SUS. In 55% of patients nodal disease was detected before referral.
Fig 2. Imaging studies that patients underwent before surgical referral.
alone before referral. In aggregate, 57% of patients were referred with a single imaging study, whereas 40% had more than 1 imaging study. Fig 3 demonstrates the percentage of radiographic studies that detected lateral neck nodal disease before referral. Overall, nodal disease was suggested by CT scan in 70.8% and by US in 47.5%. In aggregate, nodal disease was only identified in 50% of patients with 1 study and 50% of patients with more than 1 study before surgical referral. Additionally, the lag time between prereferral imaging and SUS was 1.95 ± 2.6 months (0–12 months). Furthermore, we determined that in the subset of patients diagnosed with nodal disease on SUS, 15% were referred without a tissue diagnosis (no thyroid FNA) (Fig 4). In this group of patients who were all eventually found to have thyroid cancer with lateral neck disease, 4% of patients were referred with a diagnosis of a solitary thyroid nodule to be evaluated for the need for biopsy, 7% were referred with a diagnosis of multinodular goiter. Additionally, 2% of patients were referred with a diagnosis of Graves’ disease and 2% for primary hyperparathyroidism. Of the patients referred who had an earlier thyroid FNA, a majority had a prereferral biopsy-proven diagnosis of thyroid cancer (Fig 5). However, a subset of patients were referred with nonmalignant cytology (nondiagnostic, benign, atypia of undetermined
Fig 3. Nodal detection rate of prereferral imaging studies.
Please cite this article in press as: Monteiro Rosebel, et al., Importance of surgeon-performed ultrasound in the preoperative nodal assessment of patients with potential thyroid malignancy, Surgery (2017), doi: 10.1016/j.surg.2017.10.005
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Fig 4. Reason for surgical referral or prereferral diagnoses in patients who presented with no FNA. (All patients were eventually diagnosed with metastatic thyroid cancer after SUS.).
significance, suspicious for follicular neoplasm) who were eventually found to have metastatic thyroid cancer based on SUS findings and subsequent lymph node FNA. Thus, of all patients who eventually underwent total thyroidectomy and lateral neck dissection for thyroid cancer, only 67% had a diagnosis of thyroid cancer established at the time of referral before performance of SUS. To analyze the rate of missed disease that was not identified on preoperative SUS at our institution, we evaluated patients who underwent lateral neck nodal dissection within 6 months of the initial operation for papillary thyroid cancer (group 2). During the study period, a total of 1,097 patients underwent total thyroidectomy for thyroid cancer and among those patients 10 presented at their 6-month visit with lateral neck disease, concerning for missed disease at the initial operation. This corresponds to the false negative rate of US at our institution of 0.9%. The average sonographic size of the missed malignant node was 1.56 ± 0.8 cm (0.5–3.31 cm), which was similar to the pathology report’s size of malignant lymph nodes of 1.8 ± 1 cm (0.6–2.5 cm). Discussion An increasing number of endocrine surgeons are performing cervical ultrasonography as an imaging modality in the office and in the operating room to evaluate patients with thyroid and parathy-
roid disease. When thyroid nodules are detected on physical exam, the 2016 ATA guidelines recommend that US evaluation of the anterior cervical lymph node compartments (central and lateral) be performed.9 Preoperative identification of structural disease in the lateral neck alters the preoperative discussion with the patient, increases the pretest probability of disease, and greatly influences the nature of the operation.16,17 Additionally, it has the potential to reduce the morbidity of locoregional recurrence.18 Although cervical recurrence does not predict the development of extracervical metastases and may not significantly impact survival, re-operation is costly, traumatic, and can be associated with devastating complications that impact the patients’ quality of life. At our institution, we found that, among patients referred for thyroid and parathyroid disease, prereferral imaging studies often lack details about structural neck disease despite previously established standardization criteria for reporting sonographic features of thyroid nodules and lymph nodes.19 Thus, reliance on radiographic imaging or reports alone may result in incomplete operative management as pathologic lymph nodes are often nonpalpable and operative evaluation of the lateral neck is not routine. In our study, despite the fact that most patients in this series had undergone ongoing prereferral imaging, SUS was the first study to detect lateral neck metastatic adenopathy in 45% of patients. This led to a modification of the diagnosis and a change in the planned
Fig 5. Reason for surgical referral or prereferral diagnosis in patients who presented after undergoing thyroid FNA. (All patients were eventually diagnosed with metastatic thyroid cancer after SUS.).
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operation from total thyroidectomy to include a lateral neck dissection. Additionally, 2% of patients with a prereferral diagnosis of primary hyperparathyroidism were found on the basis of SUS to have metastatic thyroid cancer. Although the number is small, SUS had a significant impact on their management as well. Thus, although knowledge of the nodal status is crucial in patients with thyroid cancer, evaluation of the nodes should be performed routinely in all referred patients. Naturally, surgeons are vigilant during preoperative US in patients presenting with a diagnosis of cancer when assessing for nodal disease or in patients with prereferral imaging suspicious of lateral neck disease; however, if SUS is standardized to survey routinely the lateral neck regardless of prereferral diagnosis, the risk of missed disease can be minimized. Although a substantial number of patients underwent various modes of prereferral imaging studies, lateral neck nodal disease was only reported in only about one half of our patients regardless of the number of imaging performed before SUS. In patients with thyroid cancer, the lag time between prereferral imaging and SUS was a median of 2 months, which still does not explain the discrepancy in the detection of lateral neck structural disease on SUS. This is most likely explained by a poor detection rate on other imaging modalities. As we are unable to control for patient and prereferral factors and a majority of these studies were not ordered by the surgeon before referral, we have standardized our SUS regardless of the prereferral diagnosis or prereferral imaging studies. Additionally, at our institution, we do not routinely order additional imaging studies before surgical referral. One of the limitations of this study is that we potentially overlooked patients with nodal disease not identified on SUS. To complete this internal validation, we evaluated the 1,097 patients who underwent total thyroidectomy for thyroid cancer at our institution between 2000 and 2016 and found 10 patients with evidence of likely persistent disease in the lateral neck at their 6-month postoperative visit. In addition to demonstrating the importance of continuing sonographic surveillance for recurrence in all patients with thyroid cancer, this also shows that SUS is not without limitations. Although the goal is to strive toward perfection, performance of US remains operator-dependent, and nodal disease still may be missed by experienced ultrasonographers. This further highlights the need for surgeons to perform a comprehensive SUS in all patients who present with thyroid disease not only to improve their ability to detect disease, but also to optimize surgical treatment. Best practices require that patients with thyroid cancer be managed by a multidisciplinary team of endocrinologists, surgeons, and radiologists. Although these resources are not necessarily available at every institution, surgeons have a broader understanding of the surgical anatomy and are uniquely qualified to stage the lateral neck. The purpose of the comprehensive SUS is to perform a complete cervical neck evaluation in patients with thyroid and parathyroid disease; however, this may not be the purpose of their prereferral imaging. Thus, the ability of surgeons to participate in the process to incorporate US widely into endocrine practice is important for patients, referring physicians, and for the improvement of the surgeons’ sonographic skills. Our data demonstrate that SUS is crucial in the preoperative evaluation of all patients referred for surgical treatment. Surgeons have a vested interest in performing a complete operation for cure in patients with thyroid cancer, and they are uniquely skilled in understanding the anatomic relationships of structures in the neck. SUS has the ability to detect additional lateral neck metastatic disease
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not only in patients with incomplete thyroid cancer staging, but also in patients referred with nonmalignant diagnoses. Reliance on standard preoperative imaging alone would have led to an incorrect initial operation in 45% of these patients who eventually underwent total thyroidectomy with lateral neck dissection for thyroid cancer. Additionally, there are several direct patient benefits to a clinical evaluation that relies on SUS as a routine part of the evaluation. Awareness of the limitations of prereferral imaging is important for surgeons when treating patients with thyroid and parathyroid disease. We have found SUS to be a useful tool in the diagnosis and accurate staging of patients and advocate for its use. References 1. Milas M, Stephen A, Berber E, Wagner K, Miskulin J, Siperstein A. Ultrasonography for the endocrine surgeon: a valuable clinical tool that enhances diagnostic and therapeutic outcomes. Surgery 2005;138:1193-200, discussion 200-1. 2. Lew JI, Solorzano CC. Use of ultrasound in the management of thyroid cancer. Oncologist 2010;15:253-8. 3. Stulak JM, Grant CS, Farley DR, et al. Value of preoperative ultrasonography in the surgical management of initial and reoperative papillary thyroid cancer. Arch Surg 2006;141:489-94, discussion 494-6. 4. Shaha AR, Shah JP, Loree TR. Patterns of nodal and distant metastasis based on histologic varieties in differentiated carcinoma of the thyroid. Am J Surg 1996;172:692-4. 5. Saad MF, Ordonez NG, Rashid RK, et al. Medullary carcinoma of the thyroid. A study of the clinical features and prognostic factors in 161 patients. Medicine (Baltimore) 1984;63:319-42. 6. Lee CY, Snyder SK, Lairmore TC, Dupont SC, Jupiter DC. Utility of surgeonperformed ultrasound assessment of the lateral neck for metastatic papillary thyroid cancer. J Oncol 2012;2012:973124. 7. Conzo G, Docimo G, Pasquali D, et al. Predictive value of nodal metastases on local recurrence in the management of differentiated thyroid cancer. Retrospective clinical study. BMC Surg 2013;13(suppl 2):S3. 8. Ito Y, Tomoda C, Uruno T, et al. Ultrasonographically and anatomopathologically detectable node metastases in the lateral compartment as indicators of worse relapse-free survival in patients with papillary thyroid carcinoma. World J Surg 2005;29:917-20. 9. Haugen BR, Alexander EK, Bible KC, et al. 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association Guidelines Task Force on thyroid nodules and differentiated thyroid cancer. Thyroid 2016;26:1-133. 10. Shirakawa T, Miyamoto Y, Yamagishi J, Fukuda K, Tada S. Color/power Doppler sonographic differential diagnosis of superficial lymphadenopathy: Metastasis, malignant lymphoma, and benign process. J Ultrasound Med 2001;20:525-32. 11. Ahuja AT, Chow L, Chick W, King W, Metreweli C. Metastatic cervical nodes in papillary carcinoma of the thyroid: ultrasound and histological correlation. Clin Radiol 1995;50:229-31. 12. Kouvaraki MA, Shapiro SE, Fornage BD, et al. Role of preoperative ultrasonography in the surgical management of patients with thyroid cancer. Surgery 2003;134:946-54, discussion 954-5. 13. Oltmann SC, Schneider DF, Chen H, Sippel RS. All thyroid ultrasound evaluations are not equal: Sonographers specialized in thyroid cancer correctly label clinical N0 disease in well differentiated thyroid cancer. Ann Surg Oncol 2015;22:422-8. 14. Leenhardt L, Erdogan MF, Hegedus L, et al. 2013 European thyroid association guidelines for cervical ultrasound scan and ultrasound-guided techniques in the postoperative management of patients with thyroid cancer. Eur Thyroid J 2013;2:147-59. 15. Stack BC Jr, Ferris RL, Goldenberg D, et al. American Thyroid Association consensus review and statement regarding the anatomy, terminology, and rationale for lateral neck dissection in differentiated thyroid cancer. Thyroid 2012;22:501-8. 16. Mazzaglia PJ. Surgeon-performed ultrasound in patients referred for thyroid disease improves patient care by minimizing performance of unnecessary procedures and optimizing surgical treatment. World J Surg 2010;34:1164-70. 17. Stephen AE, Milas M, Garner CN, Wagner KE, Siperstein AE. Use of surgeonperformed office ultrasound and parathyroid fine needle aspiration for complex parathyroid localization. Surgery 2005;138:1143-50, discussion 1150-1. 18. Kouvaraki MA, Lee JE, Shapiro SE, Sherman SI, Evans DB. Preventable reoperations for persistent and recurrent papillary thyroid carcinoma. Surgery 2004;136:1183-91. 19. Su HK, Dos Reis LL, Lupo MA, et al. Striving toward standardization of reporting of ultrasound features of thyroid nodules and lymph nodes: a multidisciplinary consensus statement. Thyroid 2014;24:1341-9.
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Discussion DR. SAREH PARANGI (Boston, MA): Thanks for this great study. I certainly think surgeon-performed ultrasound is super important in this patient population. I just have a quick question. You mentioned that CT [computed tomography] scans had a 70% sensitivity and it was the best sensitivity. I was a little bit surprised by that. That was in your preoperative imaging. What happened if you added in the surgeon-performed ultrasound into your ultrasound category? So, if you really considered preop[erative] ultrasound to include surgeon-performed ultrasound, did the sensitivity of CAT [CT] scan, was it still better than ultrasound? DR. ROSEBEL MONTEIRO: It was hard to determine what the patient was referred with, whether they were referred for the nodes identified on CT scan or whether they were referred for their thyroid cancer or other diagnoses. So, when we went back and reviewed these patients’ prereferral imaging, we included all patients who had nodes identified on a CT scan. The presence of these nodes didn’t necessarily mean that they had metastatic disease. As I mentioned, only 22% of patients were referred with a prior FNA [fine-needle aspiration] that was concerning for metastatic disease. So, overall, there were people who had studies that indicated the presence of nodes, but they were not necessarily indicative of malignancy. DR. SAREH PARANGI (Boston, MA): So when you said that CT scan had the best sensitivity at 70%, that was just for detection of nodes, not necessarily malignant nodes? DR. ROSEBEL MONTEIRO: Correct. It’s only for detection of the nodes. DR. SAREH PARANGI (Boston, MA): I think that’s important to clarify, because I think, otherwise, the take home-message could be go out and order lots of CAT scans on your patients. I just want to point out, I think there’s only one study that shows that, and I’m not in favor of that. DR. QUAN YANG DUH (San Francisco, CA): Really very nice study, and I think most of us agree with you, that surgeons should perform his or her own ultrasound for these patients. And, more importantly, I think if you’re going to follow the patient, whomever is following the patient ought to be doing the ultrasound in the first place, and the same people should be doing that. Almost half of these patients were missed on the initial ultrasound that’s done not by the surgeon. My question for you is do you have the denominator? How many patients that started with ultrasound had their lateral neck lymph nodes missed? Because it’s not 50%. Not 50% of the patients have lateral neck. So, what is the big denominator? Out of 1,000 ultrasounds, do you end up with 50 patients with lateral neck and half of those were missed? Can you tell me the big number? DR. ROSEBEL MONTEIRO: The big number was around 92 patients.
DR. QUAN YANG DUH (San Francisco, CA): So out of 92, how many had lateral neck nodes? How many in this population? Remind me. DR. ROSEBEL MONTEIRO: Again, our study population looked at all patients who had a lateral neck dissection. There were 92 patients. And then we went back and reviewed in these 92 patients what kinds of imaging they had had. Half of those patients had an ultrasound that did not reflect lateral neck nodal disease. DR. BARBRA S. MILLER (Ann Arbor, MI): I completely agree, it’s critical in my practice to do an ultrasound, and I certainly find a lot of things that haven’t been picked up. I also think we have to cut our radiology colleagues a little bit of slack, because there are different types of ultrasound examinations for the thyroid and the lateral neck. So, oftentimes what they have been asked to do, the ultrasound that they have been asked to perform, doesn’t necessarily cover the lateral neck. We have 3 different types of ultrasounds for the neck that we can order in our computer system, and that’s thyroid ultrasound, lateral neck, or thyroid cancer surveillance scan. So, the techs are doing the exam that they have been asked to do. They don’t necessarily understand the clinical context, which I think is why it’s so important for us to be able to do that comprehensive exam. So, when you’re looking at your data and that sort of thing, I think you also have to think about what were the radiologists asked to do for that exam, because, you know, they may be doing an appropriate exam, but it’s not what we want as a comprehensive exam. I also want to know basically what type of nodes were they missing? Because the things that I find that they’re not picking up are actually what we’d consider normal sized nodes that have microcalcs in them, that kind of thing, that they may not appreciate that I will pick up on. DR. ROSEBEL MONTEIRO: Thank you for your question. The types of nodes that they were missing often were pathologically abnormal lymph nodes. Because we perform an ultrasound in all of our patients, the characteristics of the lymph nodes that we picked up were not necessarily that they were enlarged nodes but they were just abnormal-appearing lymph nodes as you mentioned with microcalcifications, rounded lymph nodes that were missing the fatty hilum and things like that. DR. BARBRA S. MILLER (Ann Arbor, MI): So, the majority of what they were missing were small nodes, not big ones that are obvious? DR. ROSEBEL MONTEIRO: Well, those were nodes that we identified, and we saw our patients within a month of their prereferral ultrasound. So, theoretically it should have been the same size. So, we were looking at not only the fact whether the node was enlarged but also pathologic characteristics of the lymph nodes. DR. BARBRA S. MILLER (Ann Arbor, MI): I’m asking if there was a size breakdown. DR. ROSEBEL MONTEIRO: There was no size breakdown.
Please cite this article in press as: Discussion, Surgery (2017), doi: 10.1016/j.surg.2017.10.008
Contents lists available at ScienceDirect
Surgery j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y m s y
American Association of Endocrine Surgeons
Importance of surgeon-performed ultrasound in the preoperative nodal assessment of patients with potential thyroid malignancy Rosebel Monteiro, MD a, Amy Han, BS b, Muhammad Etiwy, MD b, Andrew Swearingen, MD b, Vikram Krishnamurthy, MD b, Judy Jin, MD b, Joyce J. Shin, MD b, Eren Berber, MD b, and Allan E. Siperstein, MD b,* a b
Department of Endocrine Surgery, The Cleveland Clinic Foundation, Cleveland, OH Case Western Reserve School of Medicine, Cleveland, OH
A R T I C L E
I N F O
Article history: Accepted 6 October 2017
Introduction. A comprehensive cervical ultrasound evaluation is essential in the operative planning of patients with thyroid disease. Reliance on radiographic reports alone may result in incomplete operative management as pathologic lymph nodes are often not palpable and evaluation of the lateral neck is not routine. This study examined the role of surgeon-performed ultrasound in the evaluation of patients who underwent lateral neck dissection for thyroid cancer. Methods. We conducted a retrospective review of a prospectively maintained database of patients who underwent therapeutic lymph node dissection for thyroid cancer between 2001 and 2016 at our tertiary referral center. All patients had surgeon-performed ultrasound preoperatively by 1 of 7 endocrine surgeons. These findings were compared with prereferral imaging studies to determine the value of surgeonperformed ultrasound to their overall treatment. Results. Of 92 patients who underwent thyroidectomy with lateral neck dissection, 97% had prereferral imaging of the neck (ultrasonography, computed tomography, positron emission tomography). Of these patients, nodal disease was suggested by computed tomography scanning in 70.8% and by ultrasonography in 54%. Of all patients, 45% had positive lateral neck nodes detected only on surgeon-performed ultrasound despite prior neck imaging. Nodal disease was identified in 50% of patients with only 1 study and 50% of patients with greater than 1 study before surgeon-performed ultrasound. Of patients with nodes detected by surgeon-performed ultrasound, only 67% had a prereferral diagnosis of thyroid cancer. Conclusions. Our data demonstrate that reliance on standard preoperative imaging alone would have led to an incorrect initial operation in 45% of our patients. Awareness of the limitations of prereferral imaging is important for surgeons treating patients with thyroid and parathyroid disease. Surgeonperformed ultrasound is a useful tool in the diagnosis and accurate staging of patients. © 2017 Elsevier Inc. All rights reserved.
Introduction Ultrasonography (US) is a noninvasive, low-cost imaging modality that has had widespread utility in the detection, diagnosis, and treatment of patients with thyroid and parathyroid disease. The value of surgeon-performed ultrasound (SUS) has broadened to include the characterization of benign and malignant thyroid disease, evaluation of the lymph nodes, performance of fine-needle aspiration (FNA) of the lesion or the lymph node, intraoperative localization of disease, as well as postoperative surveillance of recurrence.1,2 High-resolution US has previously been shown to
Presented at the 38th Annual Meeting of the American Association of Endocrine Surgeons. * Reprint requests: Allan E Siperstein, MD, Case Western Reserve School of Medicine, Cleveland, OH. E-mail: [email protected].
modify the surgical approach in up to 40% of patients with thyroid cancer.3 Cervical lymph node metastasis occurs in up to 30% of patients with papillary thyroid carcinoma,4 while medullary thyroid carcinoma demonstrates early nodal metastases in up to 50% of patients.5 Earlier studies have also demonstrated that SUS of the lateral neck is reliable with a high sensitivity and negative predictive value.6 Sonographically detectable nodal metastases in the lateral compartment have been shown to be indicators of local recurrence, as well as poorer relapse-free survival in patients with papillary thyroid cancer.7,8 Furthermore, the 2015 American Thyroid Association (ATA) guidelines recommend that US evaluation of the anterior cervical lymph node compartments (central and lateral) be performed when thyroid nodules are detected.9 Thus, in patients presenting with documented or potential thyroid cancer, accurate preoperative staging, particularly of the lateral neck, is essential for the management of all identifiable disease with a single operation. Additionally, SUS has the potential to decrease the number of costly and time-consuming appointments for the patient and reduce
https://doi.org/10.1016/j.surg.2017.10.005 0039-6060/© 2017 Elsevier Inc. All rights reserved.
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the number of expensive and invasive studies before definitive surgical treatment. Thus, surgeons should work toward a thorough preoperative staging so that the appropriate extent of surgery is performed at the initial operation. At our institution, all patients referred for thyroid or parathyroid disease routinely undergo SUS that includes a complete examination of the lymph nodes in the central (level VI) and lateral neck (levels II–V) regardless of the initial reason for referral or the presenting diagnosis. Sonographic features that should arouse suspicion of nodal metastases include round shape, increased size, irregular margins, calcifications, cystic components, peripheral vascularity, replaced fatty hilum, and heterogeneous echo texture.10,11 Our clinical observation is that in many patients, especially in patients with thyroid cancer, prereferral imaging often lacked details about structural neck nodal disease. Thus, reliance on prereferral imaging alone may result in incomplete initial preoperative staging and operative management with the potential need for a reoperation. In terms of preoperative surveillance, earlier studies have discussed the importance of preoperative cervical US and its accuracy in identifying nodal disease.12,13 It has been previously reported that central neck lymph nodes may be missed because of shadowing from tumors. However, at the time of index thyroidectomy, these central nodes are easily discovered as they are in the field of dissection. In contrast, the lateral compartment nodes are not routinely explored and are not in the operative field. Thus, accurate staging of the lateral neck is essential for planning the appropriate initial operation, as detecting lateral neck disease can address all identifiable disease in a single operation and decrease the potential for a re-operation. Earlier studies have not evaluated patients who are referred to endocrine surgeons with nodular thyroid disease or thyroid cancer with incomplete staging of the lateral neck on prereferral imaging. The purpose of this study is to systematically evaluate patients who underwent total thyroidectomy with therapeutic lateral neck dissection as the initial operation to assess the value of SUS to their overall treatment. Methods This was an institutional research board−approved retrospective analysis of patients from a prospectively maintained database. This database was queried for patients who underwent therapeutic lymph node dissection for thyroid cancer at the Cleveland Clinic from January 1, 2001, to October 31, 2016. Before surgical referral, no imaging studies are routinely ordered by our surgeons. The prereferral imaging studies in our study were generally ordered by the referring physician (endocrinologist, primary care provider, etc); whereas all patients underwent SUS preoperatively by 1 of 7 endocrine surgeons. When SUS detects lateral neck cervical lymph nodes that are sonographically suspicious for thyroid cancer, FNA of the abnormal lymph nodes is performed for cytology and washout for thyroglobulin measurement routinely in all cases.9,14 Therapeutic central (level VI and VII) or lateral neck dissection (levels II–IV [upper, middle, and lower jugular nodes] and posterior triangle nodes [level V]) is then performed after FNA detection of malignancy or via elevated nodal thyroglobulin levels (normal <1 ng/mL). Our definition of lymph node dissections aligns with the 2012 ATA consensus statement.15 Although it is ideal to suspect central neck disease preoperatively, it is our practice to forgo performing FNA of suspicious central neck lymph nodes preoperatively because they are routinely sampled intraoperatively in patients with papillary thyroid cancer. A therapeutic central neck dissection is subsequently performed when and intraoperative frozen section reveals the presence of nodal metastases. In patients who are referred with a diagnosis of papillary thyroid cancer with no sonographically identifiable lateral neck disease, the lateral compartments are not explored.
We examined a group of patients who underwent total thyroidectomy with lateral neck dissection to determine the impact of SUS in patients who may have undergone an inadequate resection as a result of unassessed lateral neck disease. For these patients, findings of SUS were compared with prereferral imaging (group 1). Additionally, to assess the quality of our nodal surveillance, we studied patients who underwent initial surgery at our institution and were found to have lateral neck nodal disease at their 6-month postoperative oncologic follow-up visit, suggesting that this was missed at initial evaluation (group 2). We made the presumption that this was missed disease rather than interval progression of aggressive or evolving disease in order to assess the quality of our nodal surveillance. A 6-month period was chosen as this is the typical time frame for the initial post-operative longitudinal tumor surveillance after potential adjuvant radioactive iodine therapy. This time frame allows for adequate thyroid-stimulating hormone (TSH) suppression and monitoring of thyroglobulin levels and facilitates performance of high-quality US after postoperative changes have settled. Demographic and clinical data, biochemical and prereferral imaging, FNA results, extent of operation performed, and pathology from institutional review board–approved databases and patients’ records were retrospectively reviewed. Results This was a series of 92 patients who underwent total thyroidectomy and lateral neck dissection at our institution (group 1). Of these patients, 92% had papillary thyroid cancer and 8% had medullary thyroid cancer. Basic demographic data and operative characteristics including gender, age, BMI, and number and size of malignant nodes on final pathology are summarized in the Table. In all patients who eventually underwent total thyroidectomy with lateral neck lymph node dissection, 45% had disease initially detected on SUS (Fig 1). In 55% of patients, nodal disease was detected before the surgeon’s evaluation. In these patients with nodal disease detected before surgical evaluation, 61% had disease detected on US, 29% on CT, and 10% on magnetic resonance imaging (MRI). Among these patients with nodal disease detected on imaging studies before referral, only 22% of patients had lymph node FNA performed before surgical referral. The remaining 78% of patients had nodes reported on prereferral imaging, but FNA was not performed. The presence of lymph nodes was commonly mentioned on CT scan reports; however, the presence of these nodes did not necessarily indicate metastatic disease as no biopsy-proven diagnosis had occurred. SUS was utilized in these cases to confirm a tissue diagnosis and to accurately stage the patient. Before referral to a surgeon, 97% of patients (89/92) underwent at least one prereferral imaging study. Eighty-nine patients underwent a total of 124 studies before referral as some patients had more than 1 imaging study (Fig 2). Seventy-four percent of the patients underwent a prereferral US with 34% of patients that underwent an isolated US study, whereas 35% had a concurrent CT scan and 5% had a concurrent MRI/PET scan. Of the remaining patients, 19% underwent CT scan alone, and 4% underwent a PET/MRI scan
Table Patient demographics Age (average in years) Body mass index (average) Papillary thyroid carcinoma Medullary thyroid carcinoma Number of lateral nymph node resected Number of malignant lymph node on pathology Size of largest malignant lymph node (average)
43 ± 16.5 (11–75) 28.6 ± 6.9 (17–55) 91.30% 8.70% 19.7 ± 13.3 9.9 ± 7.7 cm 2.3 ± 1.0 cm (0.1–5.3 cm)
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Fig 1. Distribution of patients by mode of initial detection of lateral neck nodal disease. In all patients who eventually under TT+ LND, 45% of patients had disease detected initially on SUS. In 55% of patients nodal disease was detected before referral.
Fig 2. Imaging studies that patients underwent before surgical referral.
alone before referral. In aggregate, 57% of patients were referred with a single imaging study, whereas 40% had more than 1 imaging study. Fig 3 demonstrates the percentage of radiographic studies that detected lateral neck nodal disease before referral. Overall, nodal disease was suggested by CT scan in 70.8% and by US in 47.5%. In aggregate, nodal disease was only identified in 50% of patients with 1 study and 50% of patients with more than 1 study before surgical referral. Additionally, the lag time between prereferral imaging and SUS was 1.95 ± 2.6 months (0–12 months). Furthermore, we determined that in the subset of patients diagnosed with nodal disease on SUS, 15% were referred without a tissue diagnosis (no thyroid FNA) (Fig 4). In this group of patients who were all eventually found to have thyroid cancer with lateral neck disease, 4% of patients were referred with a diagnosis of a solitary thyroid nodule to be evaluated for the need for biopsy, 7% were referred with a diagnosis of multinodular goiter. Additionally, 2% of patients were referred with a diagnosis of Graves’ disease and 2% for primary hyperparathyroidism. Of the patients referred who had an earlier thyroid FNA, a majority had a prereferral biopsy-proven diagnosis of thyroid cancer (Fig 5). However, a subset of patients were referred with nonmalignant cytology (nondiagnostic, benign, atypia of undetermined
Fig 3. Nodal detection rate of prereferral imaging studies.
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Fig 4. Reason for surgical referral or prereferral diagnoses in patients who presented with no FNA. (All patients were eventually diagnosed with metastatic thyroid cancer after SUS.).
significance, suspicious for follicular neoplasm) who were eventually found to have metastatic thyroid cancer based on SUS findings and subsequent lymph node FNA. Thus, of all patients who eventually underwent total thyroidectomy and lateral neck dissection for thyroid cancer, only 67% had a diagnosis of thyroid cancer established at the time of referral before performance of SUS. To analyze the rate of missed disease that was not identified on preoperative SUS at our institution, we evaluated patients who underwent lateral neck nodal dissection within 6 months of the initial operation for papillary thyroid cancer (group 2). During the study period, a total of 1,097 patients underwent total thyroidectomy for thyroid cancer and among those patients 10 presented at their 6-month visit with lateral neck disease, concerning for missed disease at the initial operation. This corresponds to the false negative rate of US at our institution of 0.9%. The average sonographic size of the missed malignant node was 1.56 ± 0.8 cm (0.5–3.31 cm), which was similar to the pathology report’s size of malignant lymph nodes of 1.8 ± 1 cm (0.6–2.5 cm). Discussion An increasing number of endocrine surgeons are performing cervical ultrasonography as an imaging modality in the office and in the operating room to evaluate patients with thyroid and parathy-
roid disease. When thyroid nodules are detected on physical exam, the 2016 ATA guidelines recommend that US evaluation of the anterior cervical lymph node compartments (central and lateral) be performed.9 Preoperative identification of structural disease in the lateral neck alters the preoperative discussion with the patient, increases the pretest probability of disease, and greatly influences the nature of the operation.16,17 Additionally, it has the potential to reduce the morbidity of locoregional recurrence.18 Although cervical recurrence does not predict the development of extracervical metastases and may not significantly impact survival, re-operation is costly, traumatic, and can be associated with devastating complications that impact the patients’ quality of life. At our institution, we found that, among patients referred for thyroid and parathyroid disease, prereferral imaging studies often lack details about structural neck disease despite previously established standardization criteria for reporting sonographic features of thyroid nodules and lymph nodes.19 Thus, reliance on radiographic imaging or reports alone may result in incomplete operative management as pathologic lymph nodes are often nonpalpable and operative evaluation of the lateral neck is not routine. In our study, despite the fact that most patients in this series had undergone ongoing prereferral imaging, SUS was the first study to detect lateral neck metastatic adenopathy in 45% of patients. This led to a modification of the diagnosis and a change in the planned
Fig 5. Reason for surgical referral or prereferral diagnosis in patients who presented after undergoing thyroid FNA. (All patients were eventually diagnosed with metastatic thyroid cancer after SUS.).
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operation from total thyroidectomy to include a lateral neck dissection. Additionally, 2% of patients with a prereferral diagnosis of primary hyperparathyroidism were found on the basis of SUS to have metastatic thyroid cancer. Although the number is small, SUS had a significant impact on their management as well. Thus, although knowledge of the nodal status is crucial in patients with thyroid cancer, evaluation of the nodes should be performed routinely in all referred patients. Naturally, surgeons are vigilant during preoperative US in patients presenting with a diagnosis of cancer when assessing for nodal disease or in patients with prereferral imaging suspicious of lateral neck disease; however, if SUS is standardized to survey routinely the lateral neck regardless of prereferral diagnosis, the risk of missed disease can be minimized. Although a substantial number of patients underwent various modes of prereferral imaging studies, lateral neck nodal disease was only reported in only about one half of our patients regardless of the number of imaging performed before SUS. In patients with thyroid cancer, the lag time between prereferral imaging and SUS was a median of 2 months, which still does not explain the discrepancy in the detection of lateral neck structural disease on SUS. This is most likely explained by a poor detection rate on other imaging modalities. As we are unable to control for patient and prereferral factors and a majority of these studies were not ordered by the surgeon before referral, we have standardized our SUS regardless of the prereferral diagnosis or prereferral imaging studies. Additionally, at our institution, we do not routinely order additional imaging studies before surgical referral. One of the limitations of this study is that we potentially overlooked patients with nodal disease not identified on SUS. To complete this internal validation, we evaluated the 1,097 patients who underwent total thyroidectomy for thyroid cancer at our institution between 2000 and 2016 and found 10 patients with evidence of likely persistent disease in the lateral neck at their 6-month postoperative visit. In addition to demonstrating the importance of continuing sonographic surveillance for recurrence in all patients with thyroid cancer, this also shows that SUS is not without limitations. Although the goal is to strive toward perfection, performance of US remains operator-dependent, and nodal disease still may be missed by experienced ultrasonographers. This further highlights the need for surgeons to perform a comprehensive SUS in all patients who present with thyroid disease not only to improve their ability to detect disease, but also to optimize surgical treatment. Best practices require that patients with thyroid cancer be managed by a multidisciplinary team of endocrinologists, surgeons, and radiologists. Although these resources are not necessarily available at every institution, surgeons have a broader understanding of the surgical anatomy and are uniquely qualified to stage the lateral neck. The purpose of the comprehensive SUS is to perform a complete cervical neck evaluation in patients with thyroid and parathyroid disease; however, this may not be the purpose of their prereferral imaging. Thus, the ability of surgeons to participate in the process to incorporate US widely into endocrine practice is important for patients, referring physicians, and for the improvement of the surgeons’ sonographic skills. Our data demonstrate that SUS is crucial in the preoperative evaluation of all patients referred for surgical treatment. Surgeons have a vested interest in performing a complete operation for cure in patients with thyroid cancer, and they are uniquely skilled in understanding the anatomic relationships of structures in the neck. SUS has the ability to detect additional lateral neck metastatic disease
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not only in patients with incomplete thyroid cancer staging, but also in patients referred with nonmalignant diagnoses. Reliance on standard preoperative imaging alone would have led to an incorrect initial operation in 45% of these patients who eventually underwent total thyroidectomy with lateral neck dissection for thyroid cancer. Additionally, there are several direct patient benefits to a clinical evaluation that relies on SUS as a routine part of the evaluation. Awareness of the limitations of prereferral imaging is important for surgeons when treating patients with thyroid and parathyroid disease. We have found SUS to be a useful tool in the diagnosis and accurate staging of patients and advocate for its use. References 1. Milas M, Stephen A, Berber E, Wagner K, Miskulin J, Siperstein A. Ultrasonography for the endocrine surgeon: a valuable clinical tool that enhances diagnostic and therapeutic outcomes. Surgery 2005;138:1193-200, discussion 200-1. 2. Lew JI, Solorzano CC. Use of ultrasound in the management of thyroid cancer. Oncologist 2010;15:253-8. 3. Stulak JM, Grant CS, Farley DR, et al. Value of preoperative ultrasonography in the surgical management of initial and reoperative papillary thyroid cancer. Arch Surg 2006;141:489-94, discussion 494-6. 4. Shaha AR, Shah JP, Loree TR. Patterns of nodal and distant metastasis based on histologic varieties in differentiated carcinoma of the thyroid. Am J Surg 1996;172:692-4. 5. Saad MF, Ordonez NG, Rashid RK, et al. Medullary carcinoma of the thyroid. A study of the clinical features and prognostic factors in 161 patients. Medicine (Baltimore) 1984;63:319-42. 6. Lee CY, Snyder SK, Lairmore TC, Dupont SC, Jupiter DC. Utility of surgeonperformed ultrasound assessment of the lateral neck for metastatic papillary thyroid cancer. J Oncol 2012;2012:973124. 7. Conzo G, Docimo G, Pasquali D, et al. Predictive value of nodal metastases on local recurrence in the management of differentiated thyroid cancer. Retrospective clinical study. BMC Surg 2013;13(suppl 2):S3. 8. Ito Y, Tomoda C, Uruno T, et al. Ultrasonographically and anatomopathologically detectable node metastases in the lateral compartment as indicators of worse relapse-free survival in patients with papillary thyroid carcinoma. World J Surg 2005;29:917-20. 9. Haugen BR, Alexander EK, Bible KC, et al. 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association Guidelines Task Force on thyroid nodules and differentiated thyroid cancer. Thyroid 2016;26:1-133. 10. Shirakawa T, Miyamoto Y, Yamagishi J, Fukuda K, Tada S. Color/power Doppler sonographic differential diagnosis of superficial lymphadenopathy: Metastasis, malignant lymphoma, and benign process. J Ultrasound Med 2001;20:525-32. 11. Ahuja AT, Chow L, Chick W, King W, Metreweli C. Metastatic cervical nodes in papillary carcinoma of the thyroid: ultrasound and histological correlation. Clin Radiol 1995;50:229-31. 12. Kouvaraki MA, Shapiro SE, Fornage BD, et al. Role of preoperative ultrasonography in the surgical management of patients with thyroid cancer. Surgery 2003;134:946-54, discussion 954-5. 13. Oltmann SC, Schneider DF, Chen H, Sippel RS. All thyroid ultrasound evaluations are not equal: Sonographers specialized in thyroid cancer correctly label clinical N0 disease in well differentiated thyroid cancer. Ann Surg Oncol 2015;22:422-8. 14. Leenhardt L, Erdogan MF, Hegedus L, et al. 2013 European thyroid association guidelines for cervical ultrasound scan and ultrasound-guided techniques in the postoperative management of patients with thyroid cancer. Eur Thyroid J 2013;2:147-59. 15. Stack BC Jr, Ferris RL, Goldenberg D, et al. American Thyroid Association consensus review and statement regarding the anatomy, terminology, and rationale for lateral neck dissection in differentiated thyroid cancer. Thyroid 2012;22:501-8. 16. Mazzaglia PJ. Surgeon-performed ultrasound in patients referred for thyroid disease improves patient care by minimizing performance of unnecessary procedures and optimizing surgical treatment. World J Surg 2010;34:1164-70. 17. Stephen AE, Milas M, Garner CN, Wagner KE, Siperstein AE. Use of surgeonperformed office ultrasound and parathyroid fine needle aspiration for complex parathyroid localization. Surgery 2005;138:1143-50, discussion 1150-1. 18. Kouvaraki MA, Lee JE, Shapiro SE, Sherman SI, Evans DB. Preventable reoperations for persistent and recurrent papillary thyroid carcinoma. Surgery 2004;136:1183-91. 19. Su HK, Dos Reis LL, Lupo MA, et al. Striving toward standardization of reporting of ultrasound features of thyroid nodules and lymph nodes: a multidisciplinary consensus statement. Thyroid 2014;24:1341-9.
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Discussion DR. SAREH PARANGI (Boston, MA): Thanks for this great study. I certainly think surgeon-performed ultrasound is super important in this patient population. I just have a quick question. You mentioned that CT [computed tomography] scans had a 70% sensitivity and it was the best sensitivity. I was a little bit surprised by that. That was in your preoperative imaging. What happened if you added in the surgeon-performed ultrasound into your ultrasound category? So, if you really considered preop[erative] ultrasound to include surgeon-performed ultrasound, did the sensitivity of CAT [CT] scan, was it still better than ultrasound? DR. ROSEBEL MONTEIRO: It was hard to determine what the patient was referred with, whether they were referred for the nodes identified on CT scan or whether they were referred for their thyroid cancer or other diagnoses. So, when we went back and reviewed these patients’ prereferral imaging, we included all patients who had nodes identified on a CT scan. The presence of these nodes didn’t necessarily mean that they had metastatic disease. As I mentioned, only 22% of patients were referred with a prior FNA [fine-needle aspiration] that was concerning for metastatic disease. So, overall, there were people who had studies that indicated the presence of nodes, but they were not necessarily indicative of malignancy. DR. SAREH PARANGI (Boston, MA): So when you said that CT scan had the best sensitivity at 70%, that was just for detection of nodes, not necessarily malignant nodes? DR. ROSEBEL MONTEIRO: Correct. It’s only for detection of the nodes. DR. SAREH PARANGI (Boston, MA): I think that’s important to clarify, because I think, otherwise, the take home-message could be go out and order lots of CAT scans on your patients. I just want to point out, I think there’s only one study that shows that, and I’m not in favor of that. DR. QUAN YANG DUH (San Francisco, CA): Really very nice study, and I think most of us agree with you, that surgeons should perform his or her own ultrasound for these patients. And, more importantly, I think if you’re going to follow the patient, whomever is following the patient ought to be doing the ultrasound in the first place, and the same people should be doing that. Almost half of these patients were missed on the initial ultrasound that’s done not by the surgeon. My question for you is do you have the denominator? How many patients that started with ultrasound had their lateral neck lymph nodes missed? Because it’s not 50%. Not 50% of the patients have lateral neck. So, what is the big denominator? Out of 1,000 ultrasounds, do you end up with 50 patients with lateral neck and half of those were missed? Can you tell me the big number? DR. ROSEBEL MONTEIRO: The big number was around 92 patients.
DR. QUAN YANG DUH (San Francisco, CA): So out of 92, how many had lateral neck nodes? How many in this population? Remind me. DR. ROSEBEL MONTEIRO: Again, our study population looked at all patients who had a lateral neck dissection. There were 92 patients. And then we went back and reviewed in these 92 patients what kinds of imaging they had had. Half of those patients had an ultrasound that did not reflect lateral neck nodal disease. DR. BARBRA S. MILLER (Ann Arbor, MI): I completely agree, it’s critical in my practice to do an ultrasound, and I certainly find a lot of things that haven’t been picked up. I also think we have to cut our radiology colleagues a little bit of slack, because there are different types of ultrasound examinations for the thyroid and the lateral neck. So, oftentimes what they have been asked to do, the ultrasound that they have been asked to perform, doesn’t necessarily cover the lateral neck. We have 3 different types of ultrasounds for the neck that we can order in our computer system, and that’s thyroid ultrasound, lateral neck, or thyroid cancer surveillance scan. So, the techs are doing the exam that they have been asked to do. They don’t necessarily understand the clinical context, which I think is why it’s so important for us to be able to do that comprehensive exam. So, when you’re looking at your data and that sort of thing, I think you also have to think about what were the radiologists asked to do for that exam, because, you know, they may be doing an appropriate exam, but it’s not what we want as a comprehensive exam. I also want to know basically what type of nodes were they missing? Because the things that I find that they’re not picking up are actually what we’d consider normal sized nodes that have microcalcs in them, that kind of thing, that they may not appreciate that I will pick up on. DR. ROSEBEL MONTEIRO: Thank you for your question. The types of nodes that they were missing often were pathologically abnormal lymph nodes. Because we perform an ultrasound in all of our patients, the characteristics of the lymph nodes that we picked up were not necessarily that they were enlarged nodes but they were just abnormal-appearing lymph nodes as you mentioned with microcalcifications, rounded lymph nodes that were missing the fatty hilum and things like that. DR. BARBRA S. MILLER (Ann Arbor, MI): So, the majority of what they were missing were small nodes, not big ones that are obvious? DR. ROSEBEL MONTEIRO: Well, those were nodes that we identified, and we saw our patients within a month of their prereferral ultrasound. So, theoretically it should have been the same size. So, we were looking at not only the fact whether the node was enlarged but also pathologic characteristics of the lymph nodes. DR. BARBRA S. MILLER (Ann Arbor, MI): I’m asking if there was a size breakdown. DR. ROSEBEL MONTEIRO: There was no size breakdown.
Please cite this article in press as: Discussion, Surgery (2017), doi: 10.1016/j.surg.2017.10.008