The Value of Microvascular Imaging for Triaging Indeterminate Cervical Lymph Nodes in Patients with Papillary Thyroid Carcinoma

Seongyong Lee, Ji Ye Lee, Ra Gyoung Yoon, Ji-Hoon Kim, Hyun Sook Hong, Seongyong Lee, Ji Ye Lee, Ra Gyoung Yoon, Ji-Hoon Kim, Hyun Sook Hong

Abstract

Assessment of lymph node (LN) status in patients with papillary thyroid carcinoma (PTC) is often troublesome because of cervical LNs with indeterminate US (ultrasound) features. We aimed to explore whether Superb Microvascular Imaging (SMI) could be helpful for distinguishing metastasis from indeterminate LNs when combined with power Doppler US (PDUS). From 353 consecutive patients with PTC, LNs characterized as indeterminate by PDUS were evaluated by SMI to distinguish them from metastasis. Indeterminate LNs were reclassified according to the SMI, the malignancy risk of each category was assessed, and the diagnostic performance of suspicious findings on SMI was calculated. The incidence of US-indeterminate LNs was 26.9%. Eighty PDUS-indeterminate LNs (39 proven as benign, 41 proven as malignant) were reclassified into probably benign (n = 26), indeterminate (n = 20), and suspicious (n = 34) categories according to SMI, with malignancy risks of 19.2%, 20.0%, and 94.1%, respectively. After combining SMI with PDUS, 80.8% (21/26) of probably benign LNs and 94.1% (32/34) of suspicious LNs could be correctly diagnosed as benign and metastatic, respectively. The diagnostic sensitivity, specificity, and accuracy of categorizing LNs as suspicious based on SMI were 78.1%, 94.9%, and 86.3%, respectively. In conclusion, the combination of SMI with PDUS was helpful for the accurate stratification of indeterminate LNs based on US in patients with PTC.

Keywords: Doppler; biopsy; lymph node metastasis; thyroid cancer; ultrasonography.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Reclassification of PDUS indeterminate LNs after the addition of SMI. LN—Lymph node, PDUS—Power Doppler ultrasound, SMI—Superb Microvascular Imaging.
Figure 2
Figure 2
A 42-year-old female patient with left PTC. (A) Gray-scale US showed an ovoid hypoechoic indeterminate LN with displaced hilar echogenicity in the left neck level 3. (B) On PDUS, a displaced hilar vascularity was noted. (C) On SMI, an additional peripheral vascular signal was noted in the medial peripheral portion of the LN (arrows). (D) Contrast-enhanced CT (early arterial phase, 25 s) showed focal cortical contrast enhancement in the corresponding area (arrowhead). (E) Subsequent FNA and modified radical neck dissection revealed a metastatic papillary thyroid carcinoma (H&E stain, ×200). PTC-papillary thyroid carcinoma, US—ultrasound, LN—lymph node, PDUS—power Doppler ultrasound, SMI—superb microvascular imaging, FNA—fine needle aspiration.
Figure 3
Figure 3
A 30-year-old female patient with right PTC. (A) Gray-scale US showed an ovoid hypoechoic indeterminate LN with loss of hilar echogenicity at right neck level 2. (B) Hilar vascularity was also absent on PDUS (arrow). (C) On SMI, hilar vascularity was noted in the central area of the LN. (D) Subsequent FNA and surgical biopsy revealed reactive hyperplasia (FNA-thyroglobulin = 0.16 ng/mL) (H&E stain, ×200). PTC = papillary thyroid carcinoma, US = ultrasound, LN = lymph node, PDUS = power Doppler ultrasound, SMI = superb microvascular imaging, FNA = fine needle aspiration.
Figure 4
Figure 4
Reclassified LN categories of SMI. (A) SMI probably benign LN. Grey scale and PDUS images show a hypoechoic LN with loss of hilum and hilar vascularity in the left neck level 3. On SMI, central hilar vascularity is noted (arrows), and this LN is classified as ‘SMI probably benign’ (final diagnosis-benign on FNA-Tg) (B) SMI indeterminate LN. Grey scale and PDUS show a small LN in right neck level 4 with loss of hilum and hilar vascularity. On SMI, no additional vascular signals are noted; therefore, this LN is classified as ‘SMI indeterminate’ (final diagnosis-benign on FNA-Tg). (C) SMI suspicious LN. Grey scale and PDUS show a hypoechoic LN with eccentric cortical thickening and displaced hilar vascularity in left neck level 3. On SMI, abnormal peripheral vascularity is noted at the medial portion of the LN (arrows, final diagnosis-metastatic PTC on CNB). The arrowheads in figures A, B, C indicates the margin of the LN. PTC = papillary thyroid carcinoma, US = ultrasound, LN = lymph node, PDUS = power Doppler ultrasound, SMI = superb microvascular imaging, FNA = fine needle aspiration, CNB = core needle biopsy, Tg = thyroglobulin.

References

    1. Kim E., Park J.S., Son K.R., Kim J.H., Jeon S.J., Na D.G. 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. doi: 10.1089/thy.2007.0269.
    1. Stulak J.M., Grant C.S., Farley D.R., Thompson G.B., Van Heerden J.A., Hay I.D., Reading C.C., Charboneau J.W. Value of preoperative ultrasonography in the surgical management of initial and reoperative papillary thyroid cancer. Arch. Surg. 2006;141:489–494. doi: 10.1001/archsurg.141.5.489.
    1. Al-Saif O., Farrar W.B., Bloomston M., Porter K., Ringel M.D., Kloos R.T. Long-term efficacy of lymph node reoperation for persistent papillary thyroid cancer. J. Clin. Endocrinol. Metab. 2010;95:2187–2194. doi: 10.1210/jc.2010-0063.
    1. Beasley N.J.P., Lee J., Eski S., Walfish P., Witterick I., Freeman J.L. Impact of nodal metastases on prognosis in patients with well-differentiated thyroid cancer. Arch. Otolaryngol. Head Neck Surg. 2002;128:825–828. doi: 10.1001/archotol.128.7.825.
    1. Eloy C., Santos J., Soares P., Sobrinho-Simões M. Intratumoural lymph vessel density is related to presence of lymph node metastases and separates encapsulated from infiltrative papillary thyroid carcinoma. Virchows Arch. 2011;459:595–605. doi: 10.1007/s00428-011-1161-3.
    1. Hall F.T., Freeman J.L., Asa S.L., Jackson D.G., Beasley N.J. Intratumoral Lymphatics and Lymph Node Metastases in Papillary Thyroid Carcinoma. Arch. Otolaryngol. Head Neck Surg. 2003;129:716–719. doi: 10.1001/archotol.129.7.716.
    1. Pereira F., Pereira S.S., Mesquita M., Morais T., Costa M.M., Quelhas P., Lopes C., Monteiro M.P., Leite V. Lymph node metastases in papillary and medullary thyroid carcinoma are independent of intratumoral lymphatic vessel density. Eur. Thyroid J. 2017;6:57–64. doi: 10.1159/000457794.
    1. Haugen B.R., Alexander E.K., Bible K.C., Doherty G.M., Mandel S.J., Nikiforov Y.E., Pacini F., Randolph G.W., Sawka A.M., Schlumberger M., 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. doi: 10.1089/thy.2015.0020.
    1. Lamartina L., Grani G., Biffoni M., Giacomelli L., Costante G., Lupo S., Maranghi M., Plasmati K., Sponziello M., Trulli F., et al. Risk stratification of neck lesions detected sonographically during the follow-up of differentiated thyroid cancer. J. Clin. Endocrinol. Metab. 2016;101:3036–3044. doi: 10.1210/jc.2016-1440.
    1. Gharib H., Papini E., Garber J.R., Duick D.S., Harrell R.M., Hegedus L., Paschke R., Valcavi R., Vitti P. American Association of Clinical Endocrinologists, American College of Endocrinology, and Associazione Medici Endocrinologi Medical Guidelines for Clinical Practice for the diagnosis and management of thyroid nodules—2016 Update. Endocr. Pract. 2016;22:622–639. doi: 10.4158/.
    1. Leenhardt L., Erdogan M.F., Hegedus L., Mandel S.J., Paschke R., Rago T., Russ G. 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;2:147–159. doi: 10.1159/000354537.
    1. Tessler F.N., Middleton W.D., Grant E.G., Hoang J.K., Berland L.L., Teefey S.A., Cronan J.J., Beland M.D., Desser T.S., Frates M.C., et al. ACR Thyroid Imaging, reporting and data system (TI-RADS): White paper of the ACR TI-RADS Committee. J. Am. Coll. Radiol. 2017;14:587–595. doi: 10.1016/j.jacr.2017.01.046.
    1. Shin J.H., Baek J.H., Chung J., Ha E.J., Kim J.H., Lee Y.H., Lim H.K., Moon W.J., Na D.G., Park J.S., et al. Ultrasonography diagnosis and imaging-based management of thyroid nodules: Revised Korean Society of thyroid radiology consensus statement and recommendations. Korean J. Radiol. 2016;17:370–395. doi: 10.3348/kjr.2016.17.3.370.
    1. Yoo R.E., Kim J.H., Bae J.M., Hwang I., Kang K.M., Yun T.J., Choi S.H., Sohn C.H., Rhim J.H., Park S.W. Ultrasonographic indeterminate lymph nodes in preoperative thyroid cancer patients: Malignancy risk and ultrasonographic findings predictive of malignancy. Korean J. Radiol. 2020;21:598–604. doi: 10.3348/kjr.2019.0755.
    1. Yoo R.E., Kim J.H., Hwang I., Kang K.M., Yun T.J., Choi S.H., Sohn C.H., Park S.W. Added Value of computed tomography to ultrasonography for assessing LN metastasis in preoperative patients with thyroid cancer: Node-By-Node correlation. Cancers. 2020;12:1190. doi: 10.3390/cancers12051190.
    1. Demene C., Deffieux T., Pernot M., Osmanski B.F., Biran V., Gennisson J.L., Sieu L.A., Bergel A., Franqui S., Correas J.M., et al. Spatiotemporal Clutter filtering of ultrafast ultrasound data highly increases doppler and fultrasound sensitivity. IEEE Trans. Med Imaging. 2015;34:2271–2285. doi: 10.1109/TMI.2015.2428634.
    1. Chae E.Y., Yoon G.Y., Cha J.H., Shin H.J., Choi W.J., Kim H.H. Added Value of the vascular index on superb microvascular imaging for the evaluation of breast masses: Comparison with grayscale ultrasound. J. Ultrasound Med. 2020 doi: 10.1002/jum.15441.
    1. Leong J.Y., Wessner C.E., Kramer M.R., Forsberg F., Halpern E.J., Lyshchik A., Torkzaban M., Morris A., Byrne K., VanMeter M., et al. Superb microvascular imaging improves detection of vascularity in indeterminate renal masses. J. Ultrasound Med. 2020 doi: 10.1002/jum.15299.
    1. Park A.Y., Seo B.K., Woo O.H., Jung K.S., Cho K.R., Park E.K., Cha S.H., Cha J. The utility of ultrasound superb microvascular imaging for evaluation of breast tumour vascularity: Comparison with colour and power Doppler imaging regarding diagnostic performance. Clin. Radiol. 2018;73:304–311. doi: 10.1016/j.crad.2017.10.006.
    1. Yongfeng Z., Ping Z., Hong P., Wengang L., Yan Z. Superb microvascular imaging compared with contrast-enhanced ultrasound to assess microvessels in thyroid nodules. J. Med. Ultrason. 2020;47:287–297. doi: 10.1007/s10396-020-01011-z.
    1. Bayramoglu Z., Caliskan E., Karakas Z., Karaman S., Tugcu D., Somer A., Acar M., Akıcı F., Adaletli I. Diagnostic performances of superb microvascular imaging, shear wave elastography and shape index in pediatric lymph nodes categorization: A comparative study. Br. J. Radiol. 2018;91:20180129. doi: 10.1259/bjr.20180129.
    1. Ryoo I., Suh S., You S.H., Seol H.Y. Usefulness of microvascular ultrasonography in differentiating metastatic lymphadenopathy from tuberculous lymphadenitis. Ultrasound Med. Biol. 2016;42:2189–2195. doi: 10.1016/j.ultrasmedbio.2016.05.012.
    1. Sim J.K., Lee J.Y., Hong H.S. Differentiation Between malignant and benign lymph nodes: Role of superb microvascular imaging in the evaluation of cervical lymph nodes. J. Ultrasound Med. 2019;38:3025–3036. doi: 10.1002/jum.15010.
    1. Ryoo I., Suh S., Lee Y.H., Seo H.S., Seol H.Y., Woo J.-S., Kim S.C. Vascular pattern analysis on microvascular sonography for differentiation of pleomorphic adenomas and warthin tumors of salivary glands. J. Ultrasound Med. 2018;37:613–620. doi: 10.1002/jum.14368.
    1. Bunone G., Vigneri P., Mariani L., Buto S., Collini P., Pilotti S., Pierotti M.A., Bongarzone I. Expression of angiogenesis stimulators and inhibitors in human thyroid tumors and correlation with clinical pathological features. Am. J. Pathol. 1999;155:1967–1976. doi: 10.1016/S0002-9440(10)65515-0.
    1. Turner H.E., Harris A.L., Melmed S., Wass J.A. Angiogenesis in endocrine tumors. Endocr. Rev. 2003;24:600–632. doi: 10.1210/er.2002-0008.
    1. Na D.G., Lim H.K., Byun H.S., Kim H.D., Ko Y.H., Baek J.H. Differential diagnosis of cervical lymphadenopathy: Usefulness of color Doppler sonography. Am. J. Roentgenol. 1997;168:1311–1316. doi: 10.2214/ajr.168.5.9129432.
    1. Ying M., Bhatia K.S., Lee Y.P., Yuen H.Y., Ahuja A.T. Review of ultrasonography of malignant neck nodes: Greyscale, Doppler, contrast enhancement and elastography. Cancer Imaging. 2014;13:658–669. doi: 10.1102/1470-7330.2013.0056.
    1. Leboulleux S., Girard E., Rose M., Travagli J.P., Sabbah N., Caillou B., Hartl D.M., Lassau N., Baudin E., Schlumberger M. Ultrasound criteria of malignancy for cervical lymph nodes in patients followed up for differentiated thyroid cancer. J. Clin. Endocrinol. Metab. 2007;92:3590–3594. doi: 10.1210/jc.2007-0444.
    1. Rosário P.W., De Faria S., Bicalho L., Alves M.F., Borges M.A., Purisch S., Padrão E.L., Rezende L.L., Barroso A.L. Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J. Ultrasound Med. 2005;24:1385–1389. doi: 10.7863/jum.2005.24.10.1385.
    1. Kuna S.K., Bracic I., Tesic V., Kuna K., Herceg G.H., Dodig D. Ultrasonographic differentiation of benign from malignant neck lymphadenopathy in thyroid cancer. J. Ultrasound Med. 2006;25:1531–1537. doi: 10.7863/jum.2006.25.12.1531.
    1. Sohn Y.M., Kwak J.Y., Kim E.K., Moon H.J., Kim S.J., Kim M.J. Diagnostic approach for evaluation of lymph node metastasis from thyroid cancer using ultrasound and fine-needle aspiration biopsy. AJR. Am. J. Roentgenol. 2010;194:38–43. doi: 10.2214/AJR.09.3128.
    1. Yeh M.W., Bauer A.J., Bernet V.A., Ferris R.L., Loevner L.A., Mandel S.J., Orloff L.A., Randolph G.W., Steward D.L. American Thyroid Association statement on preoperative imaging for thyroid cancer surgery. Thyroid. 2015;25:3–14. doi: 10.1089/thy.2014.0096.
    1. Ardito G., Revelli L., Giustozzi E., Salvatori M., Fadda G., Ardito F., Avenia N., Ferretti A., Rampin L., Chondrogiannis S., et al. Aggressive papillary thyroid microcarcinoma: Prognostic factors and therapeutic strategy. Clin. Nucl. Med. 2013;38:25–28. doi: 10.1097/RLU.0b013e318279bc65.
    1. Siddiqui S., White M.G., Antic T., Grogan R.H., Angelos P., Kaplan E.L., Cipriani N.A. Clinical and pathologic predictors of lymph node metastasis and recurrence in papillary thyroid microcarcinoma. Thyroid. 2016;26:807–815. doi: 10.1089/thy.2015.0429.
    1. Hoang J.K., Vanka J., Ludwig B.J., Glastonbury C.M. Evaluation of cervical lymph nodes in head and neck cancer with CT and MRI: Tips, traps, and a systematic approach. Am. J. Roentgenol. 2013;200:W17–W25. doi: 10.2214/AJR.12.8960.
    1. Moon J.H., Kim Y.I., Lim J.A., Choi H.S., Cho S.W., Kim K.W., Park H.J., Paeng J.C., Park Y.J., Yi K.H., et al. Thyroglobulin in washout fluid from lymph node fine-needle aspiration biopsy in papillary thyroid cancer: Large-scale validation of the cutoff value to determine malignancy and evaluation of discrepant results. J. Clin. Endocrinol. Metab. 2013;98:1061–1068. doi: 10.1210/jc.2012-3291.

Source: PubMed

3
Suscribir