Skip to main content
Top
Published in: European Radiology 10/2014

01-10-2014 | Head and Neck

Contrast-enhanced ultrasound (CEUS) facilitated US in detecting lateral neck lymph node metastasis of thyroid cancer patients: diagnosis value and enhancement patterns of malignant lymph nodes

Authors: Dapeng Xiang, Yurong Hong, Bo Zhang, Pintong Huang, Guogang Li, Ping Wang, Zhiyu Li

Published in: European Radiology | Issue 10/2014

Login to get access

Abstract

Objectives

To examine the value of CEUS as a non-invasive tool in detecting lateral neck metastasis (LNM) and the enhancement patterns of malignant lymph nodes (LN) for thyroid cancer patients.

Methods

Eighty-two consecutive patients, who underwent both preoperative non-enhanced US and CEUS examinations, were retrospectively reviewed. All patients underwent lateral neck dissection (LND). Enhancement patterns of 102 collected LNs matching to CEUS findings were analyzed.

Results

CEUS detected LNM in 53 of 65 patients, showing a higher sensitivity and accuracy than that of conventional US (p = 0.109 and p = 0.154, respectively). Thirteen patients’ surgical procedures were altered by CEUS findings, including nine true positive and four false positive cases. Five patients’ surgical procedures were altered by conventional US findings, including two true positive and three false positive cases. Heterogeneous enhancement, perfusion defects, microcalcification, and centripetal/hybrid enhancement were all specific criteria for malignant LNs in univariate analysis. In multivariate analysis, only heterogeneous enhancement and centripetal/hybrid enhancement were significantly related to LN metastasis (p = 0.000 and p = 0.037, respectively).

Conclusions

CEUS may be a potential tool to facilitate conventional US in detecting LNM. Heterogeneous enhancement and centripetal/hybrid enhancement are useful criteria to distinguish between malignant and benign LNs.

Key Points

• CEUS findings facilitated conventional US in detecting LNM.
• Heterogeneous, centripetal/hybrid enhancement, microcalcification and perfusion defects were specific criteria of malignant LNs.
• Heterogeneous and centripetal/hybrid enhancement were significantly related to LN metastasis in multivariate analysis.
Appendix
Available only for authorised users
Literature
1.
2.
go back to reference McGregor GI, Luoma A, Jackson SM (1985) Lymph node metastases from well-differentiated thyroid cancer. A clinical review. Am J Surg 149:610–612PubMedCrossRef McGregor GI, Luoma A, Jackson SM (1985) Lymph node metastases from well-differentiated thyroid cancer. A clinical review. Am J Surg 149:610–612PubMedCrossRef
3.
go back to reference Shaha AR, Shah JP, Loree TR (1996) Patterns of nodal and distant metastasis based on histologic varieties in differentiated carcinoma of the thyroid. Am J Surg 172:692–694PubMedCrossRef Shaha AR, Shah JP, Loree TR (1996) Patterns of nodal and distant metastasis based on histologic varieties in differentiated carcinoma of the thyroid. Am J Surg 172:692–694PubMedCrossRef
4.
go back to reference Noguchi S, Noguchi A, Murakami N (1970) Papillary carcinoma of the thyroid. I. Developing pattern of metastasis. Cancer 26:1053–1060PubMedCrossRef Noguchi S, Noguchi A, Murakami N (1970) Papillary carcinoma of the thyroid. I. Developing pattern of metastasis. Cancer 26:1053–1060PubMedCrossRef
5.
go back to reference Machens A, Hauptmann S, Dralle H (2009) Lymph node dissection in the lateral neck for completion in central node-positive papillary thyroid cancer. Surgery 145:176–181PubMedCrossRef Machens A, Hauptmann S, Dralle H (2009) Lymph node dissection in the lateral neck for completion in central node-positive papillary thyroid cancer. Surgery 145:176–181PubMedCrossRef
6.
go back to reference White ML, Gauger PG, Doherty GM (2007) Central lymph node dissection in differentiated thyroid cancer. World J Surg 31:895–904PubMedCrossRef White ML, Gauger PG, Doherty GM (2007) Central lymph node dissection in differentiated thyroid cancer. World J Surg 31:895–904PubMedCrossRef
7.
go back to reference Torlontano M, Attard M, Crocetti U et al (2004) Follow-up of low risk patients with papillary thyroid cancer: role of neck ultrasonography in detecting lymph node metastases. J Clin Endocrinol Metab 89:3402–3407PubMedCrossRef Torlontano M, Attard M, Crocetti U et al (2004) Follow-up of low risk patients with papillary thyroid cancer: role of neck ultrasonography in detecting lymph node metastases. J Clin Endocrinol Metab 89:3402–3407PubMedCrossRef
8.
go back to reference Pacini F, Molinaro E, Castagna MG et al (2003) Recombinant human thyrotropin-stimulated serum thyroglobulin combined with neck ultrasonography has the highest sensitivity in monitoring differentiated thyroid carcinoma. J Clin Endocrinol Metab 88:3668–3673PubMedCrossRef Pacini F, Molinaro E, Castagna MG et al (2003) Recombinant human thyrotropin-stimulated serum thyroglobulin combined with neck ultrasonography has the highest sensitivity in monitoring differentiated thyroid carcinoma. J Clin Endocrinol Metab 88:3668–3673PubMedCrossRef
9.
go back to reference Frasoldati A, Pesenti M, Gallo M, Caroggio A, Salvo D, Valcavi R (2003) Diagnosis of neck recurrences in patients with differentiated thyroid carcinoma. Cancer 97:90–96PubMedCrossRef Frasoldati A, Pesenti M, Gallo M, Caroggio A, Salvo D, Valcavi R (2003) Diagnosis of neck recurrences in patients with differentiated thyroid carcinoma. Cancer 97:90–96PubMedCrossRef
10.
go back to reference Roh JL, Kim JM, Park CI (2008) Lateral cervical lymph node metastases from papillary thyroid carcinoma: pattern of nodal metastases and optimal strategy for neck dissection. Ann Surg Oncol 15:1177–1182PubMedCrossRef Roh JL, Kim JM, Park CI (2008) Lateral cervical lymph node metastases from papillary thyroid carcinoma: pattern of nodal metastases and optimal strategy for neck dissection. Ann Surg Oncol 15:1177–1182PubMedCrossRef
11.
go back to reference Nemec U, Nemec SF, Novotny C, Weber M, Czerny C, Krestan CR (2012) Quantitative evaluation of contrast-enhanced ultrasound after intravenous administration of a microbubble contrast agent for differentiation of benign and malignant thyroid nodules: assessment of diagnostic accuracy. Eur Radiol 22:1357–1365PubMedCrossRef Nemec U, Nemec SF, Novotny C, Weber M, Czerny C, Krestan CR (2012) Quantitative evaluation of contrast-enhanced ultrasound after intravenous administration of a microbubble contrast agent for differentiation of benign and malignant thyroid nodules: assessment of diagnostic accuracy. Eur Radiol 22:1357–1365PubMedCrossRef
12.
go back to reference Zhang B, Jiang YX, Liu JB et al (2010) Utility of contrast-enhanced ultrasound for evaluation of thyroid nodules. Thyroid 20:51–57PubMedCrossRef Zhang B, Jiang YX, Liu JB et al (2010) Utility of contrast-enhanced ultrasound for evaluation of thyroid nodules. Thyroid 20:51–57PubMedCrossRef
13.
go back to reference Agha A, Hornung M, Rennert J et al (2011) Contrast-enhanced ultrasonography for localization of pathologic glands in patients with primary hyperparathyroidism. Surgery 151:580–586PubMedCrossRef Agha A, Hornung M, Rennert J et al (2011) Contrast-enhanced ultrasonography for localization of pathologic glands in patients with primary hyperparathyroidism. Surgery 151:580–586PubMedCrossRef
14.
go back to reference Agha A, Hornung M, Stroszczynski C, Schlitt HJ, Jung EM (2013) Highly efficient localization of pathological glands in primary hyperparathyroidism using contrast-enhanced ultrasonography (CEUS) in comparison with conventional ultrasonography. J Clin Endocrinol Metab 98:2019–2025PubMedCrossRef Agha A, Hornung M, Stroszczynski C, Schlitt HJ, Jung EM (2013) Highly efficient localization of pathological glands in primary hyperparathyroidism using contrast-enhanced ultrasonography (CEUS) in comparison with conventional ultrasonography. J Clin Endocrinol Metab 98:2019–2025PubMedCrossRef
15.
go back to reference Yu M, Liu Q, Song HP et al (2010) Clinical application of contrast-enhanced ultrasonography in diagnosis of superficial lymphadenopathy. J Ultrasound Med 29:735–740PubMed Yu M, Liu Q, Song HP et al (2010) Clinical application of contrast-enhanced ultrasonography in diagnosis of superficial lymphadenopathy. J Ultrasound Med 29:735–740PubMed
16.
go back to reference Leboulleux S, Girard E, Rose M et al (2007) Ultrasound criteria of malignancy for cervical lymph nodes in patients followed up for differentiated thyroid cancer. J Clin Endocrinol Metab 92:3590–3594PubMedCrossRef Leboulleux S, Girard E, Rose M et al (2007) Ultrasound criteria of malignancy for cervical lymph nodes in patients followed up for differentiated thyroid cancer. J Clin Endocrinol Metab 92:3590–3594PubMedCrossRef
17.
go back to reference Antonelli A, Miccoli P, Ferdeghini M et al (1995) Role of neck ultrasonography in the follow-up of patients operated on for thyroid cancer. Thyroid 5:25–28PubMedCrossRef Antonelli A, Miccoli P, Ferdeghini M et al (1995) Role of neck ultrasonography in the follow-up of patients operated on for thyroid cancer. Thyroid 5:25–28PubMedCrossRef
18.
go back to reference Rosario PW, de Faria S, Bicalho L et al (2005) Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J Ultrasound Med 24:1385–1389PubMed Rosario PW, de Faria S, Bicalho L et al (2005) Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J Ultrasound Med 24:1385–1389PubMed
19.
go back to reference Grant CS, Hay ID, Gough IR, Bergstralh EJ, Goellner JR, McConahey WM (1988) Local recurrence in papillary thyroid carcinoma: is extent of surgical resection important? Surgery 104:954–962PubMed Grant CS, Hay ID, Gough IR, Bergstralh EJ, Goellner JR, McConahey WM (1988) Local recurrence in papillary thyroid carcinoma: is extent of surgical resection important? Surgery 104:954–962PubMed
20.
go back to reference Hay ID, Thompson GB, Grant CS et al (2002) Papillary thyroid carcinoma managed at the Mayo Clinic during six decades (1940–1999): temporal trends in initial therapy and long-term outcome in 2444 consecutively treated patients. World J Surg 26:879–885PubMedCrossRef Hay ID, Thompson GB, Grant CS et al (2002) Papillary thyroid carcinoma managed at the Mayo Clinic during six decades (1940–1999): temporal trends in initial therapy and long-term outcome in 2444 consecutively treated patients. World J Surg 26:879–885PubMedCrossRef
21.
go back to reference Leboulleux S, Rubino C, Baudin E et al (2005) Prognostic factors for persistent or recurrent disease of papillary thyroid carcinoma with neck lymph node metastases and/or tumor extension beyond the thyroid capsule at initial diagnosis. J Clin Endocrinol Metab 90:5723–5729PubMedCrossRef Leboulleux S, Rubino C, Baudin E et al (2005) Prognostic factors for persistent or recurrent disease of papillary thyroid carcinoma with neck lymph node metastases and/or tumor extension beyond the thyroid capsule at initial diagnosis. J Clin Endocrinol Metab 90:5723–5729PubMedCrossRef
22.
go back to reference Yamashita H, Noguchi S, Murakami N, Kawamoto H, Watanabe S (1997) Extracapsular invasion of lymph node metastasis is an indicator of distant metastasis and poor prognosis in patients with thyroid papillary carcinoma. Cancer 80:2268–2272PubMedCrossRef Yamashita H, Noguchi S, Murakami N, Kawamoto H, Watanabe S (1997) Extracapsular invasion of lymph node metastasis is an indicator of distant metastasis and poor prognosis in patients with thyroid papillary carcinoma. Cancer 80:2268–2272PubMedCrossRef
23.
go back to reference Stulak JM, Grant CS, Farley DR et al (2006) Value of preoperative ultrasonography in the surgical management of initial and reoperative papillary thyroid cancer. Arch Surg 141:489–494, discussion 494–486PubMedCrossRef Stulak JM, Grant CS, Farley DR et al (2006) Value of preoperative ultrasonography in the surgical management of initial and reoperative papillary thyroid cancer. Arch Surg 141:489–494, discussion 494–486PubMedCrossRef
24.
go back to reference Bruneton JN, Roux P, Caramella E, Demard F, Vallicioni J, Chauvel P (1984) Ear, nose, and throat cancer: ultrasound diagnosis of metastasis to cervical lymph nodes. Radiology 152:771–773PubMedCrossRef Bruneton JN, Roux P, Caramella E, Demard F, Vallicioni J, Chauvel P (1984) Ear, nose, and throat cancer: ultrasound diagnosis of metastasis to cervical lymph nodes. Radiology 152:771–773PubMedCrossRef
25.
go back to reference Gorges R, Eising EG, Fotescu D et al (2003) Diagnostic value of high-resolution B-mode and power-mode sonography in the follow-up of thyroid cancer. Eur J Ultrasound 16:191–206PubMedCrossRef Gorges R, Eising EG, Fotescu D et al (2003) Diagnostic value of high-resolution B-mode and power-mode sonography in the follow-up of thyroid cancer. Eur J Ultrasound 16:191–206PubMedCrossRef
26.
go back to reference Pacini F, Schlumberger M, Dralle H, Elisei R, Smit JW, Wiersinga W (2006) European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. Eur J Endocrinol 154:787–803PubMedCrossRef Pacini F, Schlumberger M, Dralle H, Elisei R, Smit JW, Wiersinga W (2006) European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. Eur J Endocrinol 154:787–803PubMedCrossRef
27.
go back to reference Stack BC Jr, Ferris RL, Goldenberg D et al (2012) American Thyroid Association consensus review and statement regarding the anatomy, terminology, and rationale for lateral neck dissection in differentiated thyroid cancer. Thyroid 22:501–508PubMedCrossRef Stack BC Jr, Ferris RL, Goldenberg D et al (2012) American Thyroid Association consensus review and statement regarding the anatomy, terminology, and rationale for lateral neck dissection in differentiated thyroid cancer. Thyroid 22:501–508PubMedCrossRef
28.
go back to reference Cooper DS, Doherty GM, Haugen BR et al (2009) Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 19:1167–1214PubMedCrossRef Cooper DS, Doherty GM, Haugen BR et al (2009) Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 19:1167–1214PubMedCrossRef
29.
go back to reference Rubaltelli L, Beltrame V, Scagliori E et al. (2013) Potential use of contrast-enhanced ultrasound (CEUS) in the detection of metastatic superficial lymph nodes in melanoma patients. Ultraschall Med Rubaltelli L, Beltrame V, Scagliori E et al. (2013) Potential use of contrast-enhanced ultrasound (CEUS) in the detection of metastatic superficial lymph nodes in melanoma patients. Ultraschall Med
30.
go back to reference Rubaltelli L, Beltrame V, Tregnaghi A, Scagliori E, Frigo AC, Stramare R (2010) Contrast-enhanced ultrasound for characterizing lymph nodes with focal cortical thickening in patients with cutaneous melanoma. AJR Am J Roentgenol 196:W8–W12CrossRef Rubaltelli L, Beltrame V, Tregnaghi A, Scagliori E, Frigo AC, Stramare R (2010) Contrast-enhanced ultrasound for characterizing lymph nodes with focal cortical thickening in patients with cutaneous melanoma. AJR Am J Roentgenol 196:W8–W12CrossRef
31.
go back to reference Papini E, Guglielmi R, Bianchini A et al (2002) Risk of malignancy in nonpalpable thyroid nodules: predictive value of ultrasound and color-Doppler features. J Clin Endocrinol Metab 87:1941–1946PubMedCrossRef Papini E, Guglielmi R, Bianchini A et al (2002) Risk of malignancy in nonpalpable thyroid nodules: predictive value of ultrasound and color-Doppler features. J Clin Endocrinol Metab 87:1941–1946PubMedCrossRef
32.
go back to reference Koike E, Noguchi S, Yamashita H, Murakami T, Ohshima A, Kawamoto H (2001) Ultrasonographic characteristics of thyroid nodules: prediction of malignancy. Arch Surg 136:334–337PubMedCrossRef Koike E, Noguchi S, Yamashita H, Murakami T, Ohshima A, Kawamoto H (2001) Ultrasonographic characteristics of thyroid nodules: prediction of malignancy. Arch Surg 136:334–337PubMedCrossRef
33.
go back to reference Kouvaraki MA, Shapiro SE, Fornage BD et al (2003) Role of preoperative ultrasonography in the surgical management of patients with thyroid cancer. Surgery 134:946–954, discussion 954–945PubMedCrossRef Kouvaraki MA, Shapiro SE, Fornage BD et al (2003) Role of preoperative ultrasonography in the surgical management of patients with thyroid cancer. Surgery 134:946–954, discussion 954–945PubMedCrossRef
34.
go back to reference Rubaltelli L, Khadivi Y, Tregnaghi A et al (2004) Evaluation of lymph node perfusion using continuous mode harmonic ultrasonography with a second-generation contrast agent. J Ultrasound Med 23:829–836PubMed Rubaltelli L, Khadivi Y, Tregnaghi A et al (2004) Evaluation of lymph node perfusion using continuous mode harmonic ultrasonography with a second-generation contrast agent. J Ultrasound Med 23:829–836PubMed
35.
go back to reference Moritz JD, Ludwig A, Oestmann JW (2000) Contrast-enhanced color Doppler sonography for evaluation of enlarged cervical lymph nodes in head and neck tumors. AJR Am J Roentgenol 174:1279–1284PubMedCrossRef Moritz JD, Ludwig A, Oestmann JW (2000) Contrast-enhanced color Doppler sonography for evaluation of enlarged cervical lymph nodes in head and neck tumors. AJR Am J Roentgenol 174:1279–1284PubMedCrossRef
36.
go back to reference Na DG, Lim HK, Byun HS, Kim HD, Ko YH, Baek JH (1997) Differential diagnosis of cervical lymphadenopathy: usefulness of color Doppler sonography. AJR Am J Roentgenol 168:1311–1316PubMedCrossRef Na DG, Lim HK, Byun HS, Kim HD, Ko YH, Baek JH (1997) Differential diagnosis of cervical lymphadenopathy: usefulness of color Doppler sonography. AJR Am J Roentgenol 168:1311–1316PubMedCrossRef
37.
go back to reference Wu CH, Chang YL, Hsu WC, Ko JY, Sheen TS, Hsieh FJ (1998) Usefulness of Doppler spectral analysis and power Doppler sonography in the differentiation of cervical lymphadenopathies. AJR Am J Roentgenol 171:503–509PubMedCrossRef Wu CH, Chang YL, Hsu WC, Ko JY, Sheen TS, Hsieh FJ (1998) Usefulness of Doppler spectral analysis and power Doppler sonography in the differentiation of cervical lymphadenopathies. AJR Am J Roentgenol 171:503–509PubMedCrossRef
38.
go back to reference Wan C, Du J, Fang H, Li F, Wang L (2011) Evaluation of breast lesions by contrast enhanced ultrasound: qualitative and quantitative analysis. Eur J Radiol 81:e444–e450PubMedCrossRef Wan C, Du J, Fang H, Li F, Wang L (2011) Evaluation of breast lesions by contrast enhanced ultrasound: qualitative and quantitative analysis. Eur J Radiol 81:e444–e450PubMedCrossRef
39.
go back to reference Laumonier H, Cailliez H, Balabaud C et al (2012) Role of contrast-enhanced sonography in differentiation of subtypes of hepatocellular adenoma: correlation with MRI findings. AJR Am J Roentgenol 199:341–348PubMedCrossRef Laumonier H, Cailliez H, Balabaud C et al (2012) Role of contrast-enhanced sonography in differentiation of subtypes of hepatocellular adenoma: correlation with MRI findings. AJR Am J Roentgenol 199:341–348PubMedCrossRef
40.
go back to reference Seo YL, Yoon DY, Baek S et al (2012) Detection of neck recurrence in patients with differentiated thyroid cancer: comparison of ultrasound, contrast-enhanced CT and (18)F-FDG PET/CT using surgical pathology as a reference standard: (ultrasound vs. CT vs. (18)F-FDG PET/CT in recurrent thyroid cancer). Eur Radiol 22:2246–2254PubMedCrossRef Seo YL, Yoon DY, Baek S et al (2012) Detection of neck recurrence in patients with differentiated thyroid cancer: comparison of ultrasound, contrast-enhanced CT and (18)F-FDG PET/CT using surgical pathology as a reference standard: (ultrasound vs. CT vs. (18)F-FDG PET/CT in recurrent thyroid cancer). Eur Radiol 22:2246–2254PubMedCrossRef
41.
go back to reference Li L, Mori S, Kodama M, Sakamoto M, Takahashi S, Kodama T (2013) Enhanced sonographic imaging to diagnose lymph node metastasis: importance of blood vessel volume and density. Cancer Res 73:2082–2092PubMedCrossRef Li L, Mori S, Kodama M, Sakamoto M, Takahashi S, Kodama T (2013) Enhanced sonographic imaging to diagnose lymph node metastasis: importance of blood vessel volume and density. Cancer Res 73:2082–2092PubMedCrossRef
Metadata
Title
Contrast-enhanced ultrasound (CEUS) facilitated US in detecting lateral neck lymph node metastasis of thyroid cancer patients: diagnosis value and enhancement patterns of malignant lymph nodes
Authors
Dapeng Xiang
Yurong Hong
Bo Zhang
Pintong Huang
Guogang Li
Ping Wang
Zhiyu Li
Publication date
01-10-2014
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 10/2014
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-014-3288-5

Other articles of this Issue 10/2014

European Radiology 10/2014 Go to the issue