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Diagnostic performance of CT in detection of metastatic cervical lymph nodes in patients with thyroid cancer: a systematic review and meta-analysis

  • Se Jin Cho
  • Chong Hyun Suh
  • Jung Hwan BaekEmail author
  • Sae Rom Chung
  • Young Jun Choi
  • Jeong Hyun Lee
Computed Tomography
  • 148 Downloads

Abstract

Objectives

Although ultrasound (US) is a standard modality for the assessment of cervical lymph node metastasis in patients with thyroid cancer, there is an increasing trend in the number of articles describing the use of contrast-enhanced computed tomography (CT). The purpose of this systematic review and meta-analysis was to evaluate the diagnostic performance of CT in the diagnosis of metastatic cervical lymph nodes and to identify the parameters responsible for heterogeneity in diagnostic performance.

Methods

Ovid-MEDLINE and EMBASE databases were searched up to May 22, 2018, for studies on the diagnostic performance of CT. The pooled sensitivity and specificity of all studies were calculated. In addition, subgroup analysis and meta-regression analysis were performed to evaluate factors responsible for heterogeneity.

Results

Seventeen (6378 patients, 11,590 lymph nodes) studies were included. The pooled sensitivity was 55% (95% CI, 47–63%), and the pooled specificity was 87% (95% CI, 90–95%). Higgins I2 statistic demonstrated substantial heterogeneity in the sensitivity (I2 = 96.3%) and specificity (I2 = 93.8%). In a per-neck level subgroup analysis, the Higgins I2 statistic demonstrated reduced heterogeneity in both sensitivity and specificity. In the meta-regression analysis, variation in the CT protocols, such as contrast amount, scan phase, and reconstruction slice thickness, was a statistically significant factor causing heterogeneity.

Conclusions

CT demonstrated acceptable diagnostic performance in the pre- and postoperative diagnosis of metastatic cervical lymph nodes in patients with thyroid cancer. Variation in the CT protocols was a main factor causing heterogeneity among the included studies.

Key Points

The role of contrast-enhanced computed tomography (CT) needs to be reassessed.

CT demonstrated acceptable diagnostic performance in the diagnosis of metastatic cervical lymph nodes in patients with thyroid cancer in the meta-analysis.

Variation in the CT protocols was a main factor causing heterogeneity in the meta-regression analysis.

Keywords

Multislice computed tomography Lymph nodes Meta-analysis Thyroid cancer Papillary thyroid cancer 

Abbreviations

CT

Contrast-enhanced computed tomography

HSROC

Hierarchic summary receiver operating characteristic

PTC

Papillary thyroid carcinoma

RFA

Radiofrequency ablation

US

Ultrasound

Notes

Funding

The authors state that this work has not received any funding.

Compliance with ethical standards

Guarantor

The scientific guarantor of this publication is Jung Hwan Baek.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors (Chong Hyun Suh) has significant statistical expertise (5 years of experience in a systematic review and meta-analysis).

Informed consent

Written informed consent was not required for this study because of the nature of our study, which was a systemic review and meta-analysis.

Ethical approval

Institutional Review Board approval was not required because of the nature of our study, which was a systemic review and meta-analysis.

Methodology

• performed at one institution

Supplementary material

330_2019_6036_MOESM1_ESM.docx (17 kb)
ESM 1 (DOCX 16 kb)

References

  1. 1.
    Sivanandan R, Soo KC (2001) Pattern of cervical lymph node metastases from papillary carcinoma of the thyroid. Br J Surg 88:1241–1244CrossRefPubMedGoogle Scholar
  2. 2.
    Randolph GW, Duh QY, Heller KS et al (2012) The prognostic significance of nodal metastases from papillary thyroid carcinoma can be stratified based on the size and number of metastatic lymph nodes, as well as the presence of extranodal extension. Thyroid 22:1144–1152CrossRefPubMedGoogle Scholar
  3. 3.
    Johnson NA, Tublin ME (2008) Postoperative surveillance of differentiated thyroid carcinoma: rationale, techniques, and controversies. Radiology 249:429–444CrossRefPubMedGoogle Scholar
  4. 4.
    Robenshtok E, Fish S, Bach A, Dominguez JM, Shaha A, Tuttle RM (2012) Suspicious cervical lymph nodes detected after thyroidectomy for papillary thyroid cancer usually remain stable over years in properly selected patients. J Clin Endocrinol Metab 97:2706–2713CrossRefPubMedGoogle Scholar
  5. 5.
    Kim H, Kim TH, Choe JH et al (2017) Patterns of initial recurrence in completely resected papillary thyroid carcinoma. Thyroid 27:908–914CrossRefPubMedGoogle Scholar
  6. 6.
    Haugen BR, Alexander EK, Bible KC et al (2016) 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 26:1–133CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Yeh MW, Bauer AJ, Bernet VA et al (2015) American Thyroid Association statement on preoperative imaging for thyroid cancer surgery. Thyroid 25:3–14CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Gharib H, Papini E, Paschke R et al (2010) American Association of Clinical Endocrinologists, Associazione Medici Endocrinologi, and European Thyroid Association medical guidelines for clinical practice for the diagnosis and management of thyroid nodules: executive summary of recommendations. Endocr Pract 16:468–475CrossRefPubMedGoogle Scholar
  9. 9.
    Shin JH, Baek JH, Chung J et al (2016) Ultrasonography diagnosis and imaging-based management of thyroid nodules: revised Korean society of thyroid radiology consensus statement and recommendations. Korean J Radiol 17:370–395CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Lesnik D, Cunnane ME, Zurakowski D et al (2014) Papillary thyroid carcinoma nodal surgery directed by a preoperative radiographic map utilizing CT scan and ultrasound in all primary and reoperative patients. Head Neck 36:191–202CrossRefPubMedGoogle Scholar
  11. 11.
    Moon HJ, Kim EK, Yoon JH, Kwak JY (2012) Differences in the diagnostic performances of staging US for thyroid malignancy according to experience. Ultrasound Med Biol 38:568–573CrossRefPubMedGoogle Scholar
  12. 12.
    King AD (2008) Imaging for staging and management of thyroid cancer. Cancer Imaging 8:57–69CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Park JE, Lee JH, Ryu KH et al (2017) Improved diagnostic accuracy using arterial phase CT for lateral cervical lymph node metastasis from papillary thyroid cancer. AJNR Am J Neuroradiol 38:782–788CrossRefPubMedGoogle Scholar
  14. 14.
    Ahn JE, Lee JH, Yi JS et al (2008) Diagnostic accuracy of CT and ultrasonography for evaluating metastatic cervical lymph nodes in patients with thyroid cancer. World J Surg 32:1552–1558CrossRefPubMedGoogle Scholar
  15. 15.
    Kim TY, Shong YK (2017) Active surveillance of papillary thyroid microcarcinoma: a mini-review from Korea. Endocrinol Metab (Seoul) 32:399–406CrossRefGoogle Scholar
  16. 16.
    Tufano RP, Clayman G, Heller KS et al (2015) Management of recurrent/persistent nodal disease in patients with differentiated thyroid cancer: a critical review of the risks and benefits of surgical intervention versus active surveillance. Thyroid 25:15–27CrossRefPubMedGoogle Scholar
  17. 17.
    Padovani RP, Kasamatsu TS, Nakabashi CC et al (2012) One month is sufficient for urinary iodine to return to its baseline value after the use of water-soluble iodinated contrast agents in post-thyroidectomy patients requiring radioiodine therapy. Thyroid 22:926–930CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Sohn SY, Choi JH, Kim NK et al (2014) The impact of iodinated contrast agent administered during preoperative computed tomography scan on body iodine pool in patients with differentiated thyroid cancer preparing for radioactive iodine treatment. Thyroid 24:872–877CrossRefPubMedGoogle Scholar
  19. 19.
    Ho JD, Tsang JF, Scoggan KA, Leslie WD (2014) Urinary iodine clearance following iodinated contrast administration: a comparison of euthyroid and postthyroidectomy subjects. J Thyroid Res 2014:580569CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Mishra A, Pradhan PK, Gambhir S, Sabaretnam M, Gupta A, Babu S (2015) Preoperative contrast-enhanced computerized tomography should not delay radioiodine ablation in differentiated thyroid carcinoma patients. J Surg Res 193:731–737CrossRefPubMedGoogle Scholar
  21. 21.
    Tala Jury HP, Castagna MG, Fioravanti C, Cipri C, Brianzoni E, Pacini F (2010) Lack of association between urinary iodine excretion and successful thyroid ablation in thyroid cancer patients. J Clin Endocrinol Metab 95:230–237CrossRefPubMedGoogle Scholar
  22. 22.
    Leenhardt L, Erdogan MF, Hegedus L et al (2013) 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 2:147–159CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Suh CH, Baek JH, Choi YJ, Lee JH (2017) Performance of CT in the preoperative diagnosis of cervical lymph node metastasis in patients with papillary thyroid cancer: a systematic review and meta-analysis. AJNR Am J Neuroradiol 38:154–161CrossRefPubMedGoogle Scholar
  24. 24.
    Liberati A, Altman DG, Tetzlaff J et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med 151:W65–W94CrossRefPubMedGoogle Scholar
  25. 25.
    Choi JS, Kim J, Kwak JY, Kim MJ, Chang HS, Kim EK (2009) Preoperative staging of papillary thyroid carcinoma: comparison of ultrasound imaging and CT. AJR Am J Roentgenol 193:871–878CrossRefPubMedGoogle Scholar
  26. 26.
    Choi YJ, Yun JS, Kook SH, Jung EC, Park YL (2010) Clinical and imaging assessment of cervical lymph node metastasis in papillary thyroid carcinomas. World J Surg 34:1494–1499CrossRefPubMedGoogle Scholar
  27. 27.
    Chong A, Ha JM, Han YH et al (2017) Preoperative lymph node staging by FDG PET/CT with contrast enhancement for thyroid cancer: a multicenter study and comparison with neck CT. Clin Exp Otorhinolaryngol 10:121–128CrossRefPubMedGoogle Scholar
  28. 28.
    Eun NL, Son EJ, Kim JA, Gweon HM, Kang JH, Youk JH (2018) Comparison of the diagnostic performances of ultrasonography, CT and fine needle aspiration cytology for the prediction of lymph node metastasis in patients with lymph node dissection of papillary thyroid carcinoma: a retrospective cohort study. Int J Surg 51:145–150CrossRefPubMedGoogle Scholar
  29. 29.
    Kang JH, Jung DW, Pak KJ et al (2018) Prognostic implication of fluorine-18 fluorodeoxyglucose positron emission tomography/computed tomography in patients with recurrent papillary thyroid cancer. Head Neck 40:94–102CrossRefPubMedGoogle Scholar
  30. 30.
    Kim E, Park JS, Son KR, Kim JH, Jeon SJ, Na DG (2008) Preoperative diagnosis of cervical metastatic lymph nodes in papillary thyroid carcinoma: comparison of ultrasound, computed tomography, and combined ultrasound with computed tomography. Thyroid 18:411–418CrossRefPubMedGoogle Scholar
  31. 31.
    Kim SK, Woo JW, Park I et al (2017) Computed tomography-detected central lymph node metastasis in ultrasonography node-negative papillary thyroid carcinoma: is it really significant? Ann Surg Oncol 24:442–449CrossRefPubMedGoogle Scholar
  32. 32.
    Lee DW, Ji YB, Sung ES et al (2013) Roles of ultrasonography and computed tomography in the surgical management of cervical lymph node metastases in papillary thyroid carcinoma. Eur J Surg Oncol 39:191–196CrossRefPubMedGoogle Scholar
  33. 33.
    Lee Y, Kim JH, Baek JH et al (2018) Value of CT added to ultrasonography for the diagnosis of lymph node metastasis in patients with thyroid cancer. Head Neck.  https://doi.org/10.1002/hed.25202
  34. 34.
    Liu X, Ouyang D, Li H et al (2015) Papillary thyroid cancer: dual-energy spectral CT quantitative parameters for preoperative diagnosis of metastasis to the cervical lymph nodes. Radiology 275:167–176CrossRefPubMedGoogle Scholar
  35. 35.
    Morita S, Mizoguchi K, Suzuki M, Iizuka K (2010) The accuracy of (18)[F]-fluoro-2-deoxy-D-glucose-positron emission tomography/computed tomography, ultrasonography, and enhanced computed tomography alone in the preoperative diagnosis of cervical lymph node metastasis in patients with papillary thyroid carcinoma. World J Surg 34:2564–2569CrossRefPubMedGoogle Scholar
  36. 36.
    Na DK, Choi YJ, Choi SH, Kook SH, Park HJ (2015) Evaluation of cervical lymph node metastasis in thyroid cancer patients using real-time CT-navigated ultrasonography: preliminary study. Ultrasonography 34:39–44CrossRefPubMedGoogle Scholar
  37. 37.
    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 22:2246–2254CrossRefPubMedGoogle Scholar
  38. 38.
    Zhao Y, Li X, Li L et al (2017) Preliminary study on the diagnostic value of single-source dual energy CT in diagnosing cervical lymph node metastasis of thyroid carcinoma. J Thorac Dis 9:4758–4766CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Kim KW, Lee J, Choi SH, Huh J, Park SH (2015) Systematic review and meta-analysis of studies evaluating diagnostic test accuracy: a practical review for clinical researchers-part I. General guidance and tips. Korean J Radiol 16:1175–1187CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Deville WL, Buntinx F, Bouter LM et al (2002) Conducting systematic reviews of diagnostic studies: didactic guidelines. BMC Med Res Methodol 2:9CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Suh CH, Park SH (2016) Successful publication of systematic review and meta-analysis of studies evaluating diagnostic test accuracy. Korean J Radiol 17:5–6CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Lee J, Kim KW, Choi SH, Huh J, Park SH (2015) Systematic review and meta-analysis of studies evaluating diagnostic test accuracy: a practical review for clinical researchers-part II. Statistical methods of meta-analysis. Korean J Radiol 16:1188–1196CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Reitsma JB, Glas AS, Rutjes AW, Scholten RJ, Bossuyt PM, Zwinderman AH (2005) Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol 58:982–990CrossRefPubMedGoogle Scholar
  44. 44.
    Rutter CM, Gatsonis CA (2001) A hierarchical regression approach to meta-analysis of diagnostic test accuracy evaluations. Stat Med 20:2865–2884CrossRefPubMedGoogle Scholar
  45. 45.
    Deeks JJ, Macaskill P, Irwig L (2005) The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol 58:882–893CrossRefPubMedGoogle Scholar
  46. 46.
    Ahmed S, Ghazarian MP, Cabanillas ME et al (2017) Imaging of anaplastic thyroid carcinoma. AJNR Am J Neuroradiol.  https://doi.org/10.3174/ajnr.A5487
  47. 47.
    AlNoury MK, Almuhayawi SM, Alghamdi KB, Al-Noury KI (2015) Preoperative imaging modalities to predict the risk of regional nodal recurrence in well-differentiated thyroid cancers. Int Arch Otorhinolaryngol 19:116–120PubMedGoogle Scholar
  48. 48.
    Byun BH, Jeong UG, Hong SP et al (2012) Prediction of central lymph node metastasis from papillary thyroid microcarcinoma by 18F-fluorodeoxyglucose PET/CT and ultrasonography. Ann Nucl Med 26:471–477CrossRefPubMedGoogle Scholar
  49. 49.
    Çaǧlayan S, Urhan M, Sildiroǧlu O, Kurt Y, Önde ME, Narin Y (2009) Management of thyroid cancer associated with elevated serum thyroglobulin and negative radioiodine scanning. Turkish J Med Sci 39:693–699Google Scholar
  50. 50.
    Eisenkraft BL, Som PM (1999) The spectrum of benign and malignant etiologies of cervical node calcification. AJR Am J Roentgenol 172:1433–1437CrossRefPubMedGoogle Scholar
  51. 51.
    Giraudet AL, Vanel D, Leboulleux S et al (2007) Imaging medullary thyroid carcinoma with persistent elevated calcitonin levels. J Clin Endocrinol Metab 92:4185–4190CrossRefPubMedGoogle Scholar
  52. 52.
    Goyal N, Pakdaman M, Kamani D, Caragacianu D, Goldenberg D, Randolph GW (2017) Mapping the distribution of nodal metastases in papillary thyroid carcinoma: where exactly are the nodes? Laryngoscope 127:1959–1964CrossRefPubMedGoogle Scholar
  53. 53.
    Kim H, Na KJ, Choi JH, Ahn BC, Ahn D, Sohn JH (2016) Feasibility of FDG-PET/CT for the initial diagnosis of papillary thyroid cancer. Eur Arch Otorhinolaryngol 273:1569–1576CrossRefPubMedGoogle Scholar
  54. 54.
    Miki H, Oshimo K, Inoue H et al (1993) Diagnosis and surgical treatment of small papillary carcinomas of the thyroid gland. J Surg Oncol 54:78–80 discussion 80-71CrossRefPubMedGoogle Scholar
  55. 55.
    Rubello D, Mazzarotto R, Casara D (2000) The role of technetium-99m methoxyisobutylisonitrile scintigraphy in the planning of therapy and follow-up of patients with differentiated thyroid carcinoma after surgery. Eur J Nucl Med 27:431–440CrossRefPubMedGoogle Scholar
  56. 56.
    Rubello D, Rampin L, Nanni C et al (2008) The role of 18F-FDG PET/CT in detecting metastatic deposits of recurrent medullary thyroid carcinoma: a prospective study. Eur J Surg Oncol 34:581–586CrossRefPubMedGoogle Scholar
  57. 57.
    Szakall S Jr, Esik O, Bajzik G et al (2002) 18F-FDG PET detection of lymph node metastases in medullary thyroid carcinoma. J Nucl Med 43:66–71PubMedGoogle Scholar
  58. 58.
    Mulla M, Schulte KM (2012) Terminology inaccuracies in the interpretation of imaging results in detection of cervical lymph node metastases in papillary thyroid cancer. Endocr Connect 1:78–86CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Soler ZM, Hamilton BE, Schuff KG, Samuels MH, Cohen JI (2008) Utility of computed tomography in the detection of subclinical nodal disease in papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg 134:973–978CrossRefPubMedGoogle Scholar
  60. 60.
    Wu CW, Dionigi G, Lee KW et al (2012) Calcifications in thyroid nodules identified on preoperative computed tomography: patterns and clinical significance. Surgery 151:464–470CrossRefPubMedGoogle Scholar
  61. 61.
    Jeong HS, Baek CH, Son YI et al (2006) Integrated 18F-FDG PET/CT for the initial evaluation of cervical node level of patients with papillary thyroid carcinoma: comparison with ultrasound and contrast-enhanced CT. Clin Endocrinol (Oxf) 65:402–407CrossRefGoogle Scholar
  62. 62.
    Lee DH, Kang WJ, Seo HS et al (2009) Detection of metastatic cervical lymph nodes in recurrent papillary thyroid carcinoma: computed tomography versus positron emission tomography-computed tomography. J Comput Assist Tomogr 33:805–810CrossRefPubMedGoogle Scholar
  63. 63.
    Yoon JH, Kim JY, Moon HJ et al (2011) Contribution of computed tomography to ultrasound in predicting lateral lymph node metastasis in patients with papillary thyroid carcinoma. Ann Surg Oncol 18:1734–1741CrossRefPubMedGoogle Scholar
  64. 64.
    Jadvar H, McDougall IR, Segall GM (1998) Evaluation of suspected recurrent papillary thyroid carcinoma with [18F]fluorodeoxyglucose positron emission tomography. Nucl Med Commun 19:547–554CrossRefPubMedGoogle Scholar
  65. 65.
    Sippel RS, Chen H (2009) Controversies in the surgical management of newly diagnosed and recurrent/residual thyroid cancer. Thyroid 19:1373–1380CrossRefPubMedGoogle Scholar
  66. 66.
    Baek JH, Kim YS, Sung JY, Choi H, Lee JH (2011) Locoregional control of metastatic well-differentiated thyroid cancer by ultrasound-guided radiofrequency ablation. AJR Am J Roentgenol 197:W331–W336CrossRefPubMedGoogle Scholar
  67. 67.
    Mauri G, Cova L, Ierace T et al (2016) Treatment of metastatic lymph nodes in the neck from papillary thyroid carcinoma with percutaneous laser ablation. Cardiovasc Intervent Radiol 39:1023–1030CrossRefPubMedGoogle Scholar
  68. 68.
    Deeks JJ (2001) Systematic reviews in health care: systematic reviews of evaluations of diagnostic and screening tests. BMJ 323:157–162CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© European Society of Radiology 2019

Authors and Affiliations

  • Se Jin Cho
    • 1
  • Chong Hyun Suh
    • 1
  • Jung Hwan Baek
    • 1
    Email author
  • Sae Rom Chung
    • 1
  • Young Jun Choi
    • 1
  • Jeong Hyun Lee
    • 1
  1. 1.Department of Radiology and Research Institute of Radiology, Asan Medical CenterUniversity of Ulsan College of MedicineSeoulRepublic of Korea

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