World Journal of Surgery

, Volume 37, Issue 2, pp 385–391 | Cite as

Preoperative Prediction of Central Lymph Node Metastasis in Thyroid Papillary Microcarcinoma Using Clinicopathologic and Sonographic Features

  • Kyung-Eun Kim
  • Eun-Kyung Kim
  • Jung Hyun Yoon
  • Kyung Hwa Han
  • Hee Jung Moon
  • Jin Young KwakEmail author



The purpose of the present study was to evaluate the clinicopathologic factors and ultrasound (US) features predictive of central lymph node metastasis (LNM) in patients diagnosed with papillary thyroid microcarcinoma (PTMC).


From March 2008 to August 2008, the clinicopathologic features and preoperative US features of 483 patients who were diagnosed with conventional PTMC were included. Medical records, US features, and pathology reports of all patients were retrospectively reviewed. Univariate and multivariate analysis was performed to identify clinicopathological prognostic factors associated with central LNM. Odds ratios (OR) with relative 95 % confidence intervals (95 % CI) were calculated to determine the relevance of all potential predictors of central LNM.


Among the 483 patients with PTMC, 139 (28.8 %) patients had central LNM. The OR of significant independent factors were 2.055 (95 % CI, 1.137–3.716), 2.075 (95 % CI, 1.27–3.39), 1.71 (95 % CI, 1.073–2.724), and 15.897 (95 % CI, 4.173–60.569), respectively, for bilaterality, larger tumor size (>5 mm), extracapsular invasion, and lateral LNM. No significant association was seen among the US features of PTMC with central LNM.


Central lymph node metastasis in patients with PTMC was significantly associated with various clinicopathological factors, including larger tumor size (>5 mm), bilaterality, extracapsular invasion, and lateral LNM. When these features are detected on preoperative US, selective central compartment dissection may be helpful in patients diagnosed with PTMC.


Lymph Node Metastasis Thyroid Cancer Papillary Thyroid Carcinoma Large Tumor Size American Thyroid Association 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Conflict of interest



  1. 1.
    Tubiana M, Schlumberger M, Rougier P et al (1985) Long-term results and prognostic factors in patients with differentiated thyroid carcinoma. Cancer 55:794–804CrossRefPubMedGoogle Scholar
  2. 2.
    Samaan NA, Maheshwari YK, Nader S et al (1983) Impact of therapy for differentiated carcinoma of the thyroid: an analysis of 706 cases. J Clin Endocrinol Metab 56:1131–1138CrossRefPubMedGoogle Scholar
  3. 3.
    Jemal A, Murray T, Samuels A et al (2003) Cancer statistics, 2003. CA Cancer J Clin 53:5–26CrossRefPubMedGoogle Scholar
  4. 4.
    Wada N, Duh QY, Sugino K et al (2003) Lymph node metastasis from 259 papillary thyroid microcarcinomas: frequency, pattern of occurrence and recurrence, and optimal strategy for neck dissection. Ann Surg 237:399–407PubMedGoogle Scholar
  5. 5.
    Mirallie E, Visset J, Sagan C et al (1999) Localization of cervical node metastasis of papillary thyroid carcinoma. World J Surg 23:970–973. doi: 10.1007/s002689900609 CrossRefPubMedGoogle Scholar
  6. 6.
    Hartl DM, Travagli JP (2009) The updated American Thyroid Association Guidelines for management of thyroid nodules and differentiated thyroid cancer: a surgical perspective. Thyroid 19:1149–1151CrossRefPubMedGoogle Scholar
  7. 7.
    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 19:1167–1214CrossRefPubMedGoogle Scholar
  8. 8.
    Ito Y, Tomoda C, Uruno T et al (2004) Preoperative ultrasonographic examination for lymph node metastasis: usefulness when designing lymph node dissection for papillary microcarcinoma of the thyroid. World J Surg 28:498–501. doi: 10.1007/s00268-004-7192-z CrossRefPubMedGoogle Scholar
  9. 9.
    Choi YJ, Yun JS, Kook SH et al (2010) Clinical and imaging assessment of cervical lymph node metastasis in papillary thyroid carcinomas. World J Surg 34:1494–1499. doi: 10.1007/s00268-010-0541-1 CrossRefPubMedGoogle Scholar
  10. 10.
    Kim EK, Park CS, Chung WY et al (2002) New sonographic criteria for recommending fine-needle aspiration biopsy of nonpalpable solid nodules of the thyroid. AJR Am J Roentgenol 178:687–691PubMedGoogle Scholar
  11. 11.
    Kim E, Park JS, Son KR et al (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
  12. 12.
    Ito Y, Tomoda C, Uruno T et al (2004) Papillary microcarcinoma of the thyroid: how should it be treated? World J Surg 28:1115–1121. doi: 10.1007/s00268-004-7644-5 CrossRefPubMedGoogle Scholar
  13. 13.
    Bramley MD, Harrison BJ (1996) Papillary microcarcinoma of the thyroid gland. Br J Surg 83:1674–1683CrossRefPubMedGoogle Scholar
  14. 14.
    Harach HR, Franssila KO, Wasenius VM (1985) Occult papillary carcinoma of the thyroid. A “normal” finding in Finland. A systematic autopsy study. Cancer 56:531–538CrossRefPubMedGoogle Scholar
  15. 15.
    Pelizzo MR, Boschin IM, Toniato A et al (2004) Natural history, diagnosis, treatment and outcome of papillary thyroid microcarcinoma (PTMC): a mono-institutional 12-year experience. Nucl Med Commun 25:547–552CrossRefPubMedGoogle Scholar
  16. 16.
    Clark OH (2011) Thyroid cancer and lymph node metastases. J Surg Oncol 103:615–618CrossRefPubMedGoogle Scholar
  17. 17.
    Kouvaraki MA, Shapiro SE, Fornage BD (2003) Role of preoperative ultrasonography in the surgical management of patients with thyroid cancer. Surgery 134:946–954; discussion 950–953CrossRefPubMedGoogle Scholar
  18. 18.
    Shimamoto K, Satake H, Sawaki A et al (1998) Preoperative staging of thyroid papillary carcinoma with ultrasonography. Eur J Radiol 29:4–10CrossRefPubMedGoogle Scholar
  19. 19.
    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 32:1552–1558. doi: 10.1007/s00268-008-9588-7 CrossRefPubMedGoogle Scholar
  20. 20.
    Hwang HS, Orloff LA (2010) Efficacy of preoperative neck ultrasound in the detection of cervical lymph node metastasis from thyroid cancer. Laryngoscope 121:487–491CrossRefPubMedGoogle Scholar
  21. 21.
    Scheumann GF, Gimm O, Wegener G et al (1994) Prognostic significance and surgical management of locoregional lymph node metastases in papillary thyroid cancer. World J Surg 18:559–567. doi: 10.1007/BF00353765 CrossRefPubMedGoogle Scholar
  22. 22.
    Tisell LE, Nilsson B, Molne J et al (1996) Improved survival of patients with papillary thyroid cancer after surgical microdissection. World J Surg 20:854–859. doi: 10.1007/s002689900130 CrossRefPubMedGoogle Scholar
  23. 23.
    Bonnet S, Hartl D, Leboulleux S et al (2009) Prophylactic lymph node dissection for papillary thyroid cancer less than 2 cm: implications for radioiodine treatment. J Clin Endocrinol Metab 94:1162–1167CrossRefPubMedGoogle Scholar
  24. 24.
    White ML, Gauger PG, Doherty GM (2007) Central lymph node dissection in differentiated thyroid cancer. World J Surg 31:895–904. doi: 10.1007/s00268-006-0907-6 CrossRefPubMedGoogle Scholar
  25. 25.
    Machens A, Holzhausen HJ, Dralle H (2005) The prognostic value of primary tumor size in papillary and follicular thyroid carcinoma. Cancer 103:2269–2273CrossRefPubMedGoogle Scholar
  26. 26.
    Machens A, Hinze R, Thomusch O et al (2002) Pattern of nodal metastasis for primary and reoperative thyroid cancer. World J Surg 26:22–28. doi: 10.1007/s00268-001-0176-3 CrossRefPubMedGoogle Scholar
  27. 27.
    Katoh R, Sasaki J, Kurihara H et al (1992) Multiple thyroid involvement (intraglandular metastasis) in papillary thyroid carcinoma. A clinicopathologic study of 105 consecutive patients. Cancer 70:1585–1590CrossRefPubMedGoogle Scholar
  28. 28.
    Russell WO, Ibanez ML, Clark RL et al (1963) Thyroid carcinoma. Classification, intraglandular dissemination, and clinicopathological study based upon whole organ sections of 80 glands. Cancer 16:1425–1460CrossRefPubMedGoogle Scholar
  29. 29.
    Salter KD, Andersen PE, Cohen JI et al (2010) Central nodal metastases in papillary thyroid carcinoma based on tumor histologic type and focality. Arch Otolaryngol Head Neck Surg 136:692–696CrossRefPubMedGoogle Scholar
  30. 30.
    Xiao GZ, Gao L (2010) Central lymph node metastasis: is it a reliable indicator of lateral node involvement in papillary thyroid carcinoma? World J Surg 34:237–241. doi: 10.1007/s00268-009-0347-1 CrossRefPubMedGoogle Scholar
  31. 31.
    Moon HJ, Kim EK, Chung WY et al (2011) Minimal extrathyroidal extension in patients with papillary thyroid microcarcinoma: is it a real prognostic factor? Ann Surg Oncol 18:1916–1923CrossRefPubMedGoogle Scholar
  32. 32.
    Gimm O, Rath FW, Dralle H (1998) Pattern of lymph node metastases in papillary thyroid carcinoma. Br J Surg 85:252–254CrossRefPubMedGoogle Scholar
  33. 33.
    Deveci MS, Deveci G, LiVolsi VA et al (2007) Concordance between thyroid nodule sizes measured by ultrasound and gross pathology examination: effect on patient management. Diagn Cytopathol 35:579–583CrossRefPubMedGoogle Scholar
  34. 34.
    Kwak JY, Kim EK, Youk JH et al (2008) Extrathyroid extension of well-differentiated papillary thyroid microcarcinoma on US. Thyroid 18:609–614CrossRefPubMedGoogle Scholar
  35. 35.
    Park JS, Son KR, Na DG et al (2009) Performance of preoperative sonographic staging of papillary thyroid carcinoma based on the sixth edition of the AJCC/UICC TNM classification system. AJR Am J Roentgenol 192:66–72CrossRefPubMedGoogle Scholar
  36. 36.
    Cunha LL, Ferreira RC, Marcello MA et al (2011) Clinical and pathological implications of concurrent autoimmune thyroid disorders and papillary thyroid cancer. J Thyroid Res 2011:387062, 13 p. doi: 10.4061/2011/387062
  37. 37.
    Pellegriti G, Belfiore A, Giuffrida D et al (1998) Outcome of differentiated thyroid cancer in Graves’ patients. J Clin Endocrinol Metab 83:2805–2809CrossRefPubMedGoogle Scholar
  38. 38.
    Ozaki O, Ito K, Kobayashi K (1990) Thyroid carcinoma in Graves’ disease. World J Surg 14:437–440. doi: 10.1007/BF01658550; discussion 440–441CrossRefPubMedGoogle Scholar
  39. 39.
    Kashima K, Yokoyama S, Noguchi S et al (1998) Chronic thyroiditis as a favorable prognostic factor in papillary thyroid carcinoma. Thyroid 8:197–202CrossRefPubMedGoogle Scholar
  40. 40.
    Loh KC, Greenspan FS, Dong F et al (1999) Influence of lymphocytic thyroiditis on the prognostic outcome of patients with papillary thyroid carcinoma. J Clin Endocrinol Metab 84:458–463CrossRefPubMedGoogle Scholar
  41. 41.
    Kim EY, Kim WG, Kim WB et al (2009) Coexistence of chronic lymphocytic thyroiditis is associated with lower recurrence rates in patients with papillary thyroid carcinoma. Clin Endocrinol 71:581–586CrossRefGoogle Scholar
  42. 42.
    Gupta S, Patel A, Folstad A et al (2001) Infiltration of differentiated thyroid carcinoma by proliferating lymphocytes is associated with improved disease-free survival for children and young adults. J Clin Endocrinol Metab 86:1346–1354CrossRefPubMedGoogle Scholar
  43. 43.
    Kwak JY, Kim EK, Kim MJ et al (2009) Papillary microcarcinoma of the thyroid: predicting factors of lateral neck node metastasis. Ann Surg Oncol 16:1348–1355CrossRefPubMedGoogle Scholar
  44. 44.
    Ito Y, Kobayashi K, Tomoda C et al (2005) Ill-defined edge on ultrasonographic examination can be a marker of aggressive characteristic of papillary thyroid microcarcinoma. World J Surg 29:1007–1011. doi: 10.1007/s00268-005-7834-9 CrossRefPubMedGoogle Scholar
  45. 45.
    Choi SH, Kim EK, Kwak JY et al (2010) Interobserver and intraobserver variations in ultrasound assessment of thyroid nodules. Thyroid 20:167–172CrossRefPubMedGoogle Scholar
  46. 46.
    So YK, Son YI, Hong SD et al (2010) Subclinical lymph node metastasis in papillary thyroid microcarcinoma: a study of 551 resections. Surgery 148:526–531CrossRefPubMedGoogle Scholar
  47. 47.
    So YK, Seo MY, Son YI (2011) Prophylactic central lymph node dissection for clinically node-negative papillary thyroid microcarcinoma: influence on serum thyroglobulin level, recurrence rate, and postoperative complications. Surgery 15:192–198Google Scholar
  48. 48.
    Takebe K, Date M, Yamamoto Y et al (1994) Mass screening for thyroid cancer with ultrasonography. Karkinos 7:309–317Google Scholar
  49. 49.
    Mazzaferri EL (2012) Managing thyroid microcarcinomas. Yonsei Med J 53:1CrossRefPubMedGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2012

Authors and Affiliations

  • Kyung-Eun Kim
    • 1
  • Eun-Kyung Kim
    • 1
  • Jung Hyun Yoon
    • 2
  • Kyung Hwa Han
    • 3
  • Hee Jung Moon
    • 1
  • Jin Young Kwak
    • 1
    Email author
  1. 1.Department of RadiologyResearch Institute of Radiological Science, Yonsei University College of MedicineSeodaemoon-gu, SeoulSouth Korea
  2. 2.Department of RadiologyCHA Bundang Medical Center, College of Medicine, CHA UniversityPocheonSouth Korea
  3. 3.Department of Research AffairsYonsei University College of MedicineSeoulSouth Korea

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