Annals of Surgical Oncology

, Volume 20, Issue 3, pp 746–752 | Cite as

Multifocality and Total Tumor Diameter Predict Central Neck Lymph Node Metastases in Papillary Thyroid Microcarcinoma

  • Qunzi Zhao
  • Jie Ming
  • Chunping Liu
  • Lan Shi
  • Xia Xu
  • Xiu Nie
  • Tao Huang
Endocrine Tumors



To identify the subgroup of high-risk papillary thyroid microcarcinoma (PTMC) inclined to lymph node metastasis (LNM).


Patients who underwent total thyroidectomy with central neck dissection and had a pathologic diagnosis of PTMC between 2003 and 2010 at Wuhan Union Hospital were identified. The frequency of LNM was retrospectively analyzed according to the clinicopathological features. For multifocal lesions, total tumor diameter (TTD) was calculated as the sum of the maximal diameter of each lesion. Last, a meta-analysis was performed with respect to multifocality and LNM in the PTMCs.


The proportion of LNM was similar between multifocal PTMCs with TTD ≤ 1 cm and unifocal tumors with diameter ≤ 1 cm (37.5 vs. 30 %, P = 0.463). LNM frequency was also similar between multifocal PTMCs with 1 < TTD ≤ 2 cm (TTD greater than 1 cm but less than or equal to 2 cm) and unifocal tumors with 1 < diameter ≤ 2 cm (56.8 vs. 64.9 %, P = 0.330). However, LNM frequency was significantly higher in multifocal PTMCs with TTD > 1 cm than unifocal tumors with diameter ≤ 1 cm (60.4 vs. 30 %, P < 0.001). A meta-analysis of nine publications plus our own data with a total 1,586 PTMCs demonstrated that multifocality was significantly associated with LNM risk (odds ratio 1.9, 95 % confidence interval 1.5–2.4).


Multifocal PTMC with TTD > 1 cm has a similar risk of LNM as a clinical papillary cancer. Routine central neck dissection is recommended in this subgroup of patients.


Lymph Node Metastasis Papillary Thyroid Carcinoma Total Thyroidectomy Central Neck Capsular Invasion 
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.


  1. 1.
    Sobin L. Histological typing of thyroid tumours. Histopathology. 1990;16:513.PubMedCrossRefGoogle Scholar
  2. 2.
    Lin JD. Increased incidence of papillary thyroid microcarcinoma with decreased tumor size of thyroid cancer. Med Oncol. 2010;27:510–8.PubMedCrossRefGoogle Scholar
  3. 3.
    Chen AY, Jemal A, Ward EM. Increasing incidence of differentiated thyroid cancer in the United States, 1988–2005. Cancer. 2009;115:3801–7.PubMedCrossRefGoogle Scholar
  4. 4.
    Giordano D, Gradoni P, Oretti G, et al. Treatment and prognostic factors of papillary thyroid microcarcinoma. Clin Otolaryngol. 2010;35:118–24.PubMedCrossRefGoogle Scholar
  5. 5.
    Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA. 2006;295:2164–7.PubMedCrossRefGoogle Scholar
  6. 6.
    Kutler DI, Crummey AD, Kuhel WI. Routine central compartment lymph node dissection for patients with papillary thyroid carcinoma. Head Neck. 2012;34:260–3.PubMedCrossRefGoogle Scholar
  7. 7.
    Garrel R, Tripodi C, Cartier C, et al. Cervical lymphadenopathies signaling thyroid microcarcinoma. Case study and review of the literature. Eur Ann Otorhinolaryngol Head Neck Dis. 2011;128:115–9.Google Scholar
  8. 8.
    Xiang J, Wu Y, Li DS, et al. New clinical features of thyroid cancer in eastern China. J Visc Surg. 2010;147:e53–6.PubMedCrossRefGoogle Scholar
  9. 9.
    Moreno MA, Agarwal G, de Luna R, et al. Preoperative lateral neck ultrasonography as a long-term outcome predictor in papillary thyroid cancer. Arch Otolaryngol Head Neck Surg. 2011;137:157–62.PubMedCrossRefGoogle Scholar
  10. 10.
    Hay ID, Hutchinson ME, Gonzalez-Losada T, et al. Papillary thyroid microcarcinoma: a study of 900 cases observed in a 60-year period. Surgery. 2008;144:980–7.PubMedCrossRefGoogle Scholar
  11. 11.
    Pisanu A, Reccia I, Nardello O, et al. Risk factors for nodal metastasis and recurrence among patients with papillary thyroid microcarcinoma: differences in clinical relevance between nonincidental and incidental tumors. World J Surg. 2009;33:460–8.PubMedCrossRefGoogle Scholar
  12. 12.
    Vaisman F, Shaha A, Fish S, Tuttle R. Initial therapy with either thyroid lobectomy or total thyroidectomy without radioactive iodine remnant ablation is associated with very low rates of structural disease recurrence in properly selected patients with differentiated thyroid cancer. Clin Endocrinol (Oxf) (in press).Google Scholar
  13. 13.
    Lundgren CI, Hall P, Dickman PW, et al. Clinically significant prognostic factors for differentiated thyroid carcinoma: a population-based, nested case–control study. Cancer. 2006;106:524–31.PubMedCrossRefGoogle Scholar
  14. 14.
    Solorzano CC, Carneiro DM, Ramirez M, et al. Surgeon-performed ultrasound in the management of thyroid malignancy. Am Surg. 2004;70:576–80.PubMedGoogle Scholar
  15. 15.
    Leboulleux S, Girard E, Rose M, et al. Ultrasound criteria of malignancy for cervical lymph nodes in patients followed up for differentiated thyroid cancer. J Clin Endocrinol Metab. 2007;92:3590–4.PubMedCrossRefGoogle Scholar
  16. 16.
    Hwang HS, Orloff LA. Efficacy of preoperative neck ultrasound in the detection of cervical lymph node metastasis from thyroid cancer. Laryngoscope. 2011;121:487–91.PubMedCrossRefGoogle Scholar
  17. 17.
    Ito Y, Tomoda C, Uruno T, et al. Clinical significance of metastasis to the central compartment from papillary microcarcinoma of the thyroid. World J Surg. 2006;30:91–9.PubMedCrossRefGoogle Scholar
  18. 18.
    DeLellis RA. Pathology and genetics of tumours of endocrine organs. Lyon: World Health Organization, 2004.Google Scholar
  19. 19.
    Chun L, Ping, Li Z, Huang T. Operational mode for differentiated thyroid cancer and correlated complications. Acta Metal. Sin. 2007;27:1–856.Google Scholar
  20. 20.
    Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Accessed 1 Sep 2012.
  21. 21.
    Shao Y, Cai XJ, Gao L, et al. Clinical factors related to central compartment lymph node metastasis in papillary thyroid microcarcinoma: clinical analysis of 117 cases. Zhonghua Yi Xue Za Zhi. 2009;89:403–5.PubMedGoogle Scholar
  22. 22.
    Xu Y, Wang J. Analysis of lymph node metastasis factors in papillary thyroid microcarcinoma. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2007;21:679–82.PubMedGoogle Scholar
  23. 23.
    Wada N, Duh QY, Sugino K, et al. Lymph node metastasis from 259 papillary thyroid microcarcinomas: frequency, pattern of occurrence and recurrence, and optimal strategy for neck dissection. Ann Surg. 2003;237:399–407.PubMedGoogle Scholar
  24. 24.
    Lim YC, Choi EC, Yoon YH, et al. Central lymph node metastases in unilateral papillary thyroid microcarcinoma. Br J Surg. 2009;96:253–7.PubMedCrossRefGoogle Scholar
  25. 25.
    Wang Y, Ji QH, Huang CP, et al. Predictive factors for level VI lymph node metastasis in papillary thyroid microcarcinoma. Zhonghua Wai Ke Za Zhi. 2008;46:1899–901.PubMedGoogle Scholar
  26. 26.
    Ito Y, Miyauchi A. Lateral lymph node dissection guided by preoperative and intraoperative findings in differentiated thyroid carcinoma. World J Surg. 2008;32:729–39.PubMedCrossRefGoogle Scholar
  27. 27.
    So YK, Son YI, Hong SD, et al. Subclinical lymph node metastasis in papillary thyroid microcarcinoma: a study of 551 resections. Surgery. 2010;148:526–31.PubMedCrossRefGoogle Scholar
  28. 28.
    Lee SH, Lee SS, Jin SM, et al. Predictive factors for central compartment lymph node metastasis in thyroid papillary microcarcinoma. Laryngoscope. 2008;118:659–62.PubMedCrossRefGoogle Scholar
  29. 29.
    Barbaro D, Simi U, Meucci G, et al. Thyroid papillary cancers: microcarcinoma and carcinoma, incidental cancers and non-incidental cancers—are they different diseases? Clin Endocrinol (Oxf). 2005;63:577–81.CrossRefGoogle Scholar
  30. 30.
    Ogilvie JB, Patel KN, Heller KS. Impact of the 2009 American Thyroid Association guidelines on the choice of operation for well-differentiated thyroid microcarcinomas. Surgery. 2010;148:1222–6.PubMedCrossRefGoogle Scholar
  31. 31.
    Mercante G, Frasoldati A, Pedroni C, et al. Prognostic factors affecting neck lymph node recurrence and distant metastasis in papillary microcarcinoma of the thyroid: results of a study in 445 patients. Thyroid. 2009;19:707–16.PubMedCrossRefGoogle Scholar
  32. 32.
    Connor MP, Wells D, Schmalbach CE. Variables predictive of bilateral occult papillary microcarcinoma following total thyroidectomy. Otolaryngol Head Neck Surg. 2011;144:210–5.PubMedCrossRefGoogle Scholar
  33. 33.
    Dunki-Jacobs E, Grannan K, McDonough S, et al. Clinically unsuspected papillary microcarcinomas of the thyroid: a common finding with favorable biology? Am J Surg. 2012;203:140–4.PubMedCrossRefGoogle Scholar
  34. 34.
    Siassakos D, Gourgiotis S, Moustafellos P, et al. Thyroid microcarcinoma during thyroidectomy. Singapore Med J. 2008;49:23–5.PubMedGoogle Scholar
  35. 35.
    Ciuffreda L, De Martino D, Bonfitto N, et al. Our experience on surgical treatment of papillary thyroid microcarcinoma. G Chir. 2011;32:41–4.PubMedGoogle Scholar
  36. 36.
    Lombardi CP, Bellantone R, De Crea C, et al. Papillary thyroid microcarcinoma: extrathyroidal extension, lymph node metastases, and risk factors for recurrence in a high prevalence of goiter area. World J Surg. 2010;34:1214–21.PubMedCrossRefGoogle Scholar
  37. 37.
    Gulben K, Berberoglu U, Celen O, et al. Incidental papillary microcarcinoma of the thyroid—factors affecting lymph node metastasis. Langenbecks Arch Surg. 2008;393:25–9.PubMedCrossRefGoogle Scholar
  38. 38.
    Chow SM, Law SC, Chan JK, et al. Papillary microcarcinoma of the thyroid—prognostic significance of lymph node metastasis and multifocality. Cancer. 2003;98:31–40.PubMedCrossRefGoogle Scholar
  39. 39.
    Yang GC, LiVolsi VA, Baloch ZW. Thyroid microcarcinoma: fine-needle aspiration diagnosis and histologic follow-up. Int J Surg Pathol. 2002;10:133–9.PubMedCrossRefGoogle Scholar
  40. 40.
    Neuhold N, Schultheis A, Hermann M, et al. Incidental papillary microcarcinoma of the thyroid—further evidence of a very low malignant potential: a retrospective clinicopathological study with up to 30 years of follow-up. Ann Surg Oncol. 2011;18:3430–6.PubMedCrossRefGoogle Scholar
  41. 41.
    Jacquot-Laperriere S, Timoshenko AP, Dumollard JM, et al. Papillary thyroid microcarcinoma: incidence and prognostic factors. Eur Arch Otorhinolaryngol. 2007;264:935–9.PubMedCrossRefGoogle Scholar
  42. 42.
    Besic N, Pilko G, Petric R, et al. Papillary thyroid microcarcinoma: prognostic factors and treatment. J Surg Oncol. 2008;97:221–5.PubMedCrossRefGoogle Scholar
  43. 43.
    Lin JD, Chao TC, Hsueh C, et al. High recurrent rate of multicentric papillary thyroid carcinoma. Ann Surg Oncol. 2009;16:2609–16.PubMedCrossRefGoogle Scholar
  44. 44.
    Page C, Biet A, Boute P, et al. “Aggressive papillary” thyroid microcarcinoma. Eur Arch Otorhinolaryngol. 2009;266:1959–63.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2012

Authors and Affiliations

  • Qunzi Zhao
    • 1
  • Jie Ming
    • 1
  • Chunping Liu
    • 1
  • Lan Shi
    • 1
  • Xia Xu
    • 2
  • Xiu Nie
    • 2
  • Tao Huang
    • 1
  1. 1.Department of General SurgeryAffiliated Union Hospital, Tongji Medical CollegeWuhanChina
  2. 2.Department of PathologyAffiliated Union Hospital, Tongji Medical CollegeWuhanChina

Personalised recommendations