CASE REPORT
Jonathan Irish, MD, FRCSC, Section Editor
Benign intranodal thyroid tissue mimicking nodal metastasis in a patient with papillary thyroid carcinoma: A case report Yoo Jin Lee, MD,1 Dong Wook Kim, MD,1* Ha Kyoung Park, MD,2 Tae Kwun Ha, MD,2 Do Hun Kim, MD,3 Soo Jin Jung, MD,4 Sang Kyun Bae, MD5 1
Department of Radiology, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea, 2Department of General Surgery, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea, 3Department of Otorhinolaryngology–Head and Neck Surgery, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea, 4Department of Pathology, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea, 5Department of Nuclear Medicine, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea.
Accepted 27 September 2014 Published online 4 June 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.23886
ABSTRACT: Background. A case of benign intranodal thyroid tissue mimicking nodal metastasis on ultrasound and CT in a patient with papillary thyroid carcinoma has not been reported. Methods. The clinical, imaging, and histopathological findings of the patient are presented. A 52-year-old woman who underwent ultrasound-guided fine-needle aspiration for 2 small, suspicious thyroid nodules in both lobes at a local clinic was referred to our hospital for surgical treatment. Ultrasound-guided fine-needle aspiration for a suspicious lymph node in the left upper neck was performed. According to the imaging and cytology results, total thyroidectomy
INTRODUCTION According to autopsy and neck dissection-based studies, since the first report of intranodal inclusion of benign thyroid tissue in 1897, its prevalence in the neck has ranged from 0.6% to 5.0%.1–3 The origin of intranodal thyroid tissue is not clear, but several hypotheses, including aberrant migration of benign tissues during embryogenesis, neoplastic transformation of resident cells, or metastatic spread from some clinically silent malignancy, have been suggested.1–4 To the best of our knowledge, a case of benign intranodal thyroid tissue mimicking lymph node metastasis on neck ultrasound and CT in a patient with papillary thyroid carcinoma has not been reported. Furthermore, no previous study has used radiological findings of intranodal inclusion of benign thyroid follicles. In this report, we present a case of benign intranodal thyroid tissue mimicking nodal metastasis in the neck on preoperative ultrasound and CT images in a patient with papillary thyroid carcinoma.
CASE REPORT In August 2013, a 52-year-old woman with papillary thyroid carcinoma who underwent ultrasound-guided
*Corresponding author: D. W. Kim, Department of Radiology, Busan Paik Hospital, Inje University College of Medicine, 633-165, Gaegeum-dong, Busanjin-gu, Busan, South Korea 614–734. E-mail: [email protected]
E106
HEAD & NECK—DOI 10.1002/HED
SEPTEMBER 2015
and nodal dissection for both central and left lateral nodes were performed. Results. In the histopathology, the lymph node was confirmed as a benign lymph node with intranodal thyroid tissue. Conclusion. This case illustrates that benign intranodal thyroid tissue may mimic nodal metastasis on ultrasound or CT in a patient with papillary thyroid carciC 2015 Wiley Periodicals, Inc. Head Neck 37: E106–E108, 2015 noma. V
KEY WORDS: lymph node, metastasis, papillary thyroid carcinoma, ultrasound, CT
fine-needle aspiration for 2 small, suspicious thyroid nodules in both lobes at a local clinic was referred to our hospital for surgical treatment. The patient showed normal values on a thyroid function test (T3 5 128.2 ng/dL; free T4 5 1.06 ng/dL; thyroid-stimulating hormone 5 2.35 mIU/L). No specific abnormalities were detected on a physical examination of the neck, and there was no history of tuberculous infection. For tumor staging, she underwent preoperative neck ultrasound. Neck ultrasound was performed by a radiologist with 12 years of experience using a high-resolution ultrasound instrument (iU 22; Philips Medical Systems, Bothell, WA) equipped with a 5 to 12 MHz linear probe. On preoperative neck ultrasound, known malignant thyroid nodules in both lobes, 2 small solid thyroid nodules in both thyroid lobes, and a suspicious malignant lymph node in the left upper neck were detected (Figure 1A and 1B). Because of the suspicious sonographic features, ultrasound-guided fine-needle aspiration for the lymph node was immediately performed by the same radiologist. However, a thyroglobulin measurement of aspirated specimen was not done. In the cytological analysis, nodal metastasis from papillary thyroid carcinoma could not be ruled out, although only benign follicular cells were observed (Figure 1C). For nodal staging, sequential preoperative neck CT was performed using a 64-channel multidetector CT scanner (Aquilion One; Toshiba Medical Systems, Otawara, Japan) with contrast medium injection (130 mL iopamidol [Pamiray 370]; Dongkook Pharmaceutical Seoul, South
BENIGN
INTRANODAL THYROID TISSUE
FIGURE 1. Benign intranodal thyroid tissue mimicking nodal metastasis in the left neck of a 52-year-old woman with papillary thyroid microcarcinoma. Longitudinal gray-scale sonograms (A) show a lymph node (arrows) with focally increased echogenicity and calcifications (arrowheads) in the left upper neck (level III, 5.4 3 9.7 3 19.8 mm). Longitudinal color Doppler sonogram (B) of the lymph node in the left upper neck reveals peripheral vascularity. In cytology (C), the aspirate obtained in ultrasound-guided fine-needle aspiration reveals some clusters of follicular cells showing slightly nuclear enlargement admixed with benign lymphoid cells. For nodal staging, preoperative neck CT was sequentially performed, and the suspicious lymph node in the left upper neck shows intranodal calcifications and increased enhancement in contrast-enhanced axial image (arrows) (D). In the histopathology of the left upper neck node (arrows), half of the lymph node is replaced by benign thyroid follicular cells (arrowheads; hematoxylin and eosin stain, original magnification 310) (E), and the thyroid follicular cells show mild nuclear enlargement and irregularity but no definite evidence of nuclear grooves or pseudo-inclusions suspecting papillary thyroid carcinoma (hematoxylin and eosin stain; original magnification 3200) (F).
Korea; 2.5 mL/s; delay 5 45 seconds). The suspicious lymph node in the left upper neck corresponded to that on the neck ultrasound (Figure 1D), but there were no other suspicious lymph nodes on the neck CT. On the basis of the imaging and cytology findings, total thyroidectomy and nodal dissection for both central and left lateral nodes were performed. Histopathology revealed 4 papillary thyroid microcarcinomas (follicular variant) and several nodular hyperplasias in both thyroid lobes, underlying lymphocytic thyroiditis, and no malignant lymph nodes (Figure 1E and 1F). Sonographically and cytologically, a suspicious malignant lymph node in the left upper neck was confirmed as a benign lymph node containing intranodal thyroid tissue. The patient was discharged after surgery without radioiodine therapy, and
she is receiving thyroid hormone replacement therapy without any complications.
DISCUSSION The origin of nodal inclusion of thyroid tissue is not completely understood. The theory of remnants of thyroid tissue, separated during embryological development, becoming entrapped in the lymph node during embryogenesis has been proposed.5 Some investigators have proposed that the inclusion of unencapsulated thyroid tissue in the jugular lymph sacs, which eventually gives rise to the cervical lymph nodes, could justify the appearance of benign thyroid tissue in the cervical lymph nodes.6 However, others have suggested that an alteration in the HEAD & NECK—DOI 10.1002/HED
SEPTEMBER 2015
E107
LEE ET AL.
embryological development of the ultimobranchial body, abnormalities in the descent, or failure of fusion of the ultimobranchial body may play a role in the appearance of benign thyroid tissue in the neck.7 Nevertheless, there are no published studies regarding the imaging features of this entity. According to the literature, the sonographic features suggestive of metastatic lymph nodes from papillary thyroid carcinoma include focally or diffusely increased nodal echogenicity, intranodal calcifications, intranodal cystic component(s), and an abnormal vascular pattern (a chaotic or peripheral vascular pattern), whereas the CT features include strong enhancement without hilar vessel enhancement, heterogeneous enhancement, intranodal calcifications, and intranodal cystic component(s).8–10 In a study by Kim et al,10 lymph nodes with an intranodal echogenic island (ie, focally increased nodal echogenicity) showed a high malignancy rate (43.8%; 7 of 16), although this was lower than that of lymph nodes with diffusely increased echogenicity (74.3%; 26 of 35). Kim et al10 hypothesized that intranodal echogenic islands indicated a localized tumor colony within a lymph node, possibly originating from the lymphatic vessels and developing through very slow growth. In addition, they suggested that the lower malignancy rate of lymph nodes with intranodal echogenic islands may be related to the diversity in the shape of normal nodal hilum or other benign conditions. In particular, benign intranodal thyroid tissue may result in false-positive cases during imaging diagnosis. However, the prevalence of sonographic detection of benign intranodal thyroid tissue in the neck has not been reported, although its prevalence in autopsy and neck dissection-based studies ranges from 0.6% to 5.0%.
E108
HEAD & NECK—DOI 10.1002/HED
SEPTEMBER 2015
CONCLUSION We have reported a case of benign intranodal thyroid tissue mimicking nodal metastasis on preoperative neck ultrasound and CT in a patient with papillary thyroid carcinoma who underwent unnecessary left lateral neck dissection because of a false-positive diagnosis from both imaging and cytological analyses. Therefore, we should be aware that benign intranodal thyroid tissue may result in false-positive nodal metastasis during imaging or cytological diagnosis in patients with papillary thyroid carcinoma.
REFERENCES 1. Fisher CJ, Hill S, Millis RR. Benign lymph node inclusions mimicking metastatic carcinoma. J Clin Pathol 1994;47:245–247. 2. Baisden BL, Askin FB, Lange JR, Westra WH. HMB-45 immunohistochemical staining of sentinel lymph nodes: a specific method for enhancing detection of micrometastases in patients with melanoma. Am J Surg Pathol 2000;24:1140–1146. 3. Ansari–Lari MA, Westra WH. The prevalence and significance of clinically unsuspected neoplasms in cervical lymph nodes. Head Neck 2003;25: 841–847. 4. Reich O, Tamussino K, Haas J, Winter R. Benign m€ ullerian inclusions in pelvic and paraaortic lymph nodes. Gynecol Oncol 2000;78:242–244. 5. Block MA, Wylie JH, Patton RB, Miller JM. Does benign thyroid tissue occur in the lateral part of the neck? Am J Surg 1966;112:476–481. 6. Meyer JS, Steinberg LS. Microscopically benign thyroid follicles in cervical lymph nodes. Serial section study of lymph node inclusions and entire thyroid gland in 5 cases. Cancer 1969;24:302–311. 7. Williams ED, Toyn CE, Harach HR. The ultimobranchial gland and congenital thyroid abnormalities in man. J Pathol 1989;159:135–141. 8. Rosario PW, de Faria S, Bicalho L, et al. Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J Ultrasound Med 2005;24:1385–1389. 9. Kim E, Park JS, Son KR, Kim JH, Jeon SJ, Na DG. Preoperative diagnosis of cervical metastatic lymph nodes in papillary thyroid carcinoma: comparison of ultrasound, computed tomography, and combined ultrasound with computed tomography. Thyroid 2008;18:411–418. 10. Kim DW, Choo HJ, Lee YJ, Jung SJ, Eom JW, Ha TK. Sonographic features of cervical lymph nodes after thyroidectomy for papillary thyroid carcinoma. J Ultrasound Med 2013;32:1173–1180.
Jonathan Irish, MD, FRCSC, Section Editor
Benign intranodal thyroid tissue mimicking nodal metastasis in a patient with papillary thyroid carcinoma: A case report Yoo Jin Lee, MD,1 Dong Wook Kim, MD,1* Ha Kyoung Park, MD,2 Tae Kwun Ha, MD,2 Do Hun Kim, MD,3 Soo Jin Jung, MD,4 Sang Kyun Bae, MD5 1
Department of Radiology, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea, 2Department of General Surgery, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea, 3Department of Otorhinolaryngology–Head and Neck Surgery, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea, 4Department of Pathology, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea, 5Department of Nuclear Medicine, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea.
Accepted 27 September 2014 Published online 4 June 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.23886
ABSTRACT: Background. A case of benign intranodal thyroid tissue mimicking nodal metastasis on ultrasound and CT in a patient with papillary thyroid carcinoma has not been reported. Methods. The clinical, imaging, and histopathological findings of the patient are presented. A 52-year-old woman who underwent ultrasound-guided fine-needle aspiration for 2 small, suspicious thyroid nodules in both lobes at a local clinic was referred to our hospital for surgical treatment. Ultrasound-guided fine-needle aspiration for a suspicious lymph node in the left upper neck was performed. According to the imaging and cytology results, total thyroidectomy
INTRODUCTION According to autopsy and neck dissection-based studies, since the first report of intranodal inclusion of benign thyroid tissue in 1897, its prevalence in the neck has ranged from 0.6% to 5.0%.1–3 The origin of intranodal thyroid tissue is not clear, but several hypotheses, including aberrant migration of benign tissues during embryogenesis, neoplastic transformation of resident cells, or metastatic spread from some clinically silent malignancy, have been suggested.1–4 To the best of our knowledge, a case of benign intranodal thyroid tissue mimicking lymph node metastasis on neck ultrasound and CT in a patient with papillary thyroid carcinoma has not been reported. Furthermore, no previous study has used radiological findings of intranodal inclusion of benign thyroid follicles. In this report, we present a case of benign intranodal thyroid tissue mimicking nodal metastasis in the neck on preoperative ultrasound and CT images in a patient with papillary thyroid carcinoma.
CASE REPORT In August 2013, a 52-year-old woman with papillary thyroid carcinoma who underwent ultrasound-guided
*Corresponding author: D. W. Kim, Department of Radiology, Busan Paik Hospital, Inje University College of Medicine, 633-165, Gaegeum-dong, Busanjin-gu, Busan, South Korea 614–734. E-mail: [email protected]
E106
HEAD & NECK—DOI 10.1002/HED
SEPTEMBER 2015
and nodal dissection for both central and left lateral nodes were performed. Results. In the histopathology, the lymph node was confirmed as a benign lymph node with intranodal thyroid tissue. Conclusion. This case illustrates that benign intranodal thyroid tissue may mimic nodal metastasis on ultrasound or CT in a patient with papillary thyroid carciC 2015 Wiley Periodicals, Inc. Head Neck 37: E106–E108, 2015 noma. V
KEY WORDS: lymph node, metastasis, papillary thyroid carcinoma, ultrasound, CT
fine-needle aspiration for 2 small, suspicious thyroid nodules in both lobes at a local clinic was referred to our hospital for surgical treatment. The patient showed normal values on a thyroid function test (T3 5 128.2 ng/dL; free T4 5 1.06 ng/dL; thyroid-stimulating hormone 5 2.35 mIU/L). No specific abnormalities were detected on a physical examination of the neck, and there was no history of tuberculous infection. For tumor staging, she underwent preoperative neck ultrasound. Neck ultrasound was performed by a radiologist with 12 years of experience using a high-resolution ultrasound instrument (iU 22; Philips Medical Systems, Bothell, WA) equipped with a 5 to 12 MHz linear probe. On preoperative neck ultrasound, known malignant thyroid nodules in both lobes, 2 small solid thyroid nodules in both thyroid lobes, and a suspicious malignant lymph node in the left upper neck were detected (Figure 1A and 1B). Because of the suspicious sonographic features, ultrasound-guided fine-needle aspiration for the lymph node was immediately performed by the same radiologist. However, a thyroglobulin measurement of aspirated specimen was not done. In the cytological analysis, nodal metastasis from papillary thyroid carcinoma could not be ruled out, although only benign follicular cells were observed (Figure 1C). For nodal staging, sequential preoperative neck CT was performed using a 64-channel multidetector CT scanner (Aquilion One; Toshiba Medical Systems, Otawara, Japan) with contrast medium injection (130 mL iopamidol [Pamiray 370]; Dongkook Pharmaceutical Seoul, South
BENIGN
INTRANODAL THYROID TISSUE
FIGURE 1. Benign intranodal thyroid tissue mimicking nodal metastasis in the left neck of a 52-year-old woman with papillary thyroid microcarcinoma. Longitudinal gray-scale sonograms (A) show a lymph node (arrows) with focally increased echogenicity and calcifications (arrowheads) in the left upper neck (level III, 5.4 3 9.7 3 19.8 mm). Longitudinal color Doppler sonogram (B) of the lymph node in the left upper neck reveals peripheral vascularity. In cytology (C), the aspirate obtained in ultrasound-guided fine-needle aspiration reveals some clusters of follicular cells showing slightly nuclear enlargement admixed with benign lymphoid cells. For nodal staging, preoperative neck CT was sequentially performed, and the suspicious lymph node in the left upper neck shows intranodal calcifications and increased enhancement in contrast-enhanced axial image (arrows) (D). In the histopathology of the left upper neck node (arrows), half of the lymph node is replaced by benign thyroid follicular cells (arrowheads; hematoxylin and eosin stain, original magnification 310) (E), and the thyroid follicular cells show mild nuclear enlargement and irregularity but no definite evidence of nuclear grooves or pseudo-inclusions suspecting papillary thyroid carcinoma (hematoxylin and eosin stain; original magnification 3200) (F).
Korea; 2.5 mL/s; delay 5 45 seconds). The suspicious lymph node in the left upper neck corresponded to that on the neck ultrasound (Figure 1D), but there were no other suspicious lymph nodes on the neck CT. On the basis of the imaging and cytology findings, total thyroidectomy and nodal dissection for both central and left lateral nodes were performed. Histopathology revealed 4 papillary thyroid microcarcinomas (follicular variant) and several nodular hyperplasias in both thyroid lobes, underlying lymphocytic thyroiditis, and no malignant lymph nodes (Figure 1E and 1F). Sonographically and cytologically, a suspicious malignant lymph node in the left upper neck was confirmed as a benign lymph node containing intranodal thyroid tissue. The patient was discharged after surgery without radioiodine therapy, and
she is receiving thyroid hormone replacement therapy without any complications.
DISCUSSION The origin of nodal inclusion of thyroid tissue is not completely understood. The theory of remnants of thyroid tissue, separated during embryological development, becoming entrapped in the lymph node during embryogenesis has been proposed.5 Some investigators have proposed that the inclusion of unencapsulated thyroid tissue in the jugular lymph sacs, which eventually gives rise to the cervical lymph nodes, could justify the appearance of benign thyroid tissue in the cervical lymph nodes.6 However, others have suggested that an alteration in the HEAD & NECK—DOI 10.1002/HED
SEPTEMBER 2015
E107
LEE ET AL.
embryological development of the ultimobranchial body, abnormalities in the descent, or failure of fusion of the ultimobranchial body may play a role in the appearance of benign thyroid tissue in the neck.7 Nevertheless, there are no published studies regarding the imaging features of this entity. According to the literature, the sonographic features suggestive of metastatic lymph nodes from papillary thyroid carcinoma include focally or diffusely increased nodal echogenicity, intranodal calcifications, intranodal cystic component(s), and an abnormal vascular pattern (a chaotic or peripheral vascular pattern), whereas the CT features include strong enhancement without hilar vessel enhancement, heterogeneous enhancement, intranodal calcifications, and intranodal cystic component(s).8–10 In a study by Kim et al,10 lymph nodes with an intranodal echogenic island (ie, focally increased nodal echogenicity) showed a high malignancy rate (43.8%; 7 of 16), although this was lower than that of lymph nodes with diffusely increased echogenicity (74.3%; 26 of 35). Kim et al10 hypothesized that intranodal echogenic islands indicated a localized tumor colony within a lymph node, possibly originating from the lymphatic vessels and developing through very slow growth. In addition, they suggested that the lower malignancy rate of lymph nodes with intranodal echogenic islands may be related to the diversity in the shape of normal nodal hilum or other benign conditions. In particular, benign intranodal thyroid tissue may result in false-positive cases during imaging diagnosis. However, the prevalence of sonographic detection of benign intranodal thyroid tissue in the neck has not been reported, although its prevalence in autopsy and neck dissection-based studies ranges from 0.6% to 5.0%.
E108
HEAD & NECK—DOI 10.1002/HED
SEPTEMBER 2015
CONCLUSION We have reported a case of benign intranodal thyroid tissue mimicking nodal metastasis on preoperative neck ultrasound and CT in a patient with papillary thyroid carcinoma who underwent unnecessary left lateral neck dissection because of a false-positive diagnosis from both imaging and cytological analyses. Therefore, we should be aware that benign intranodal thyroid tissue may result in false-positive nodal metastasis during imaging or cytological diagnosis in patients with papillary thyroid carcinoma.
REFERENCES 1. Fisher CJ, Hill S, Millis RR. Benign lymph node inclusions mimicking metastatic carcinoma. J Clin Pathol 1994;47:245–247. 2. Baisden BL, Askin FB, Lange JR, Westra WH. HMB-45 immunohistochemical staining of sentinel lymph nodes: a specific method for enhancing detection of micrometastases in patients with melanoma. Am J Surg Pathol 2000;24:1140–1146. 3. Ansari–Lari MA, Westra WH. The prevalence and significance of clinically unsuspected neoplasms in cervical lymph nodes. Head Neck 2003;25: 841–847. 4. Reich O, Tamussino K, Haas J, Winter R. Benign m€ ullerian inclusions in pelvic and paraaortic lymph nodes. Gynecol Oncol 2000;78:242–244. 5. Block MA, Wylie JH, Patton RB, Miller JM. Does benign thyroid tissue occur in the lateral part of the neck? Am J Surg 1966;112:476–481. 6. Meyer JS, Steinberg LS. Microscopically benign thyroid follicles in cervical lymph nodes. Serial section study of lymph node inclusions and entire thyroid gland in 5 cases. Cancer 1969;24:302–311. 7. Williams ED, Toyn CE, Harach HR. The ultimobranchial gland and congenital thyroid abnormalities in man. J Pathol 1989;159:135–141. 8. Rosario PW, de Faria S, Bicalho L, et al. Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J Ultrasound Med 2005;24:1385–1389. 9. Kim E, Park JS, Son KR, Kim JH, Jeon SJ, Na DG. Preoperative diagnosis of cervical metastatic lymph nodes in papillary thyroid carcinoma: comparison of ultrasound, computed tomography, and combined ultrasound with computed tomography. Thyroid 2008;18:411–418. 10. Kim DW, Choo HJ, Lee YJ, Jung SJ, Eom JW, Ha TK. Sonographic features of cervical lymph nodes after thyroidectomy for papillary thyroid carcinoma. J Ultrasound Med 2013;32:1173–1180.
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