Encapsulation Status of Papillary Thyroid Microcarcinomas is Associated with the Risk of Lymph Node Metastases and Tumor Multifocality

K. Cupisti; N. Lehwald; M. Anlauf; J. Riemer; T. A. Werner; A. Krieg; J. Witte; A. Chanab; S. E. Baldus; M. Krausch; A. Raffel; C. Herdter; M. Schott; W. T. Knoefel

doi:10.1055/s-0033-1361158

Hormone and Metabolic Research, Table of Contents

Horm Metab Res 2014; 46(02): 138-144
DOI: 10.1055/s-0033-1361158

Humans, Clinical

Encapsulation Status of Papillary Thyroid Microcarcinomas is Associated with the Risk of Lymph Node Metastases and Tumor Multifocality

K. Cupisti^*

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

N. Lehwald^*

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

M. Anlauf

²Institute of Pathology, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

J. Riemer

²Institute of Pathology, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

T. A. Werner

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

A. Krieg

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

J. Witte

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

A. Chanab

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

S. E. Baldus

²Institute of Pathology, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

M. Krausch

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

A. Raffel

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

C. Herdter

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

M. Schott

³Department of Endocrinology, Rheumatology and Diabetes, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

,

W. T. Knoefel

¹Department of General, Visceral and Pediatric Surgery, Heinrich Heine University and University Hospital Duesseldorf, Duesseldorf, Germany

› Author Affiliations

Abstract

The management of papillary microcarcinoma (PMC) of the thyroid is controversial, especially after partial thyroid resection for benign thyroid disease. In order to detect prognostic factors for PMC, we analyzed 116 patients with PMC for encapsulation status and lymph node metastases. Between 10/1992 and 12/2010, 116 patients with PMC have been operated in our department (87 females, 29 males, median age 49 years). Eighty per cent of PMCs were diagnosed postoperatively. Seventy-six patients (66%) received a more extended resection with either thyroidectomy, near total thyroidectomy, or Dunhill operation either primarily or after completion operation, whereas 40 patients (34%) had only partial resection. Fifty patients (43%) received radioiodine (RIA) ablation. Lymph node metastases were found in 21 patients (18%). Univariate analysis showed four risk factors to be significantly associated with the risk of lymph node metastasis (p<0.05): male gender, younger age, age group<50 years and nonencapsulation of the tumor. Multivariate analysis demonstrated statistical significance for gender and tumor capsulation status. The tumor capsulation status also correlated with tumor multifocality. Our data show that the risk of lymph node metastases is significantly higher in partially or nonencapsulated PMC than in encapsulated specimens. We therefore suggest that the WHO classification should be extended to a compulsory notification of the encapsulation status in PMC.

Key words

benign thyroid goiter - thyroidectomy - papillary microcarcinoma - lymph node

Full Text

References

References
1 Grodski S, Delbridge L. An update on papillary microcarcinoma. Curr Opin Oncol 2009; 21: 1-4
2 Ito Y, Uruno T, Nakano K. An observation trial without surgical treatment in patients with papillary microcarcinoma of the thyroid. Thyroid 2003; 13: 381-387
3 Noguchi S, Yamashita H, Uchino S, Watanabe S. Papillary microcarcinoma. World J Surg 2008; 32: 747-753
4 Pellegriti G, Scollo C, Lumera G, Regalbuto C, Vigneri R, Belfiore A. Clinical behavior and outcome of papillary thyroid cancers smaller than 1.5 cm in diameter: study of 299 cases. J Clin Endocrinol Metab 2004; 89: 3713-3720
5 Carcangiu ML, Zampi G, Pupi A. Papillary carcinoma of the thyroid. A clinicopathologic study of 241 cases treated at the University of Florence, Italy. Cancer 1985; 55: 805-828
6 Pisanu A, Deplano D, Reccia I, Porceddu G, Uccheddu A. Encapsulated papillary thyroid carcinoma: is it a distinctive clinical entity with low grade malignancy?. J Endocrinol Invest 2013; 36: 78-83
7 Rosai J, Ackerman LV. Rosai and Ackerman’s surgical pathology. 9th ed. Edinburgh: Mosby; 2004
8 Baldus SE, Schaefer KL, Hartleb D, Stoecklein NH, Gabbert HE. Prevalence and heterogeneity of KRAS, BRAF, and PIK3CA mutations in primary colorectal adenocarcinomas and their corresponding metastases. Clin Cancer Res 2010; 16: 790-799
9 Luca AC, Mersch S, Deenen R, Schmidt S, Messner I, Schäfer KL, Baldus SE, Huckenbeck W, Piekorz RP, Knoefel WT, Krieg A, Stoecklein NH. Impact of the 3D microenvironment on phenotype, gene expression, and EGFR inhibition of colorectal cancer cell lines. PLoS One 2013; 8: e59689
10 Chow S, Law SCK, Chan JK, Au SK, Yau S, Lau WH. Papillary microcarcinoma of the thyroid-Prognostic significance of lymph node metastasis and multifocality. Cancer 2003; 98: 31-40
11 Vorländer C, Lienenlüke RH, Wahl RA. Lymphknotendissektion beim papillären und follikulären Schilddrüsenkarzinom. Chirurg 2008; 79: 564-570
12 Kim TY, Hong SJ, Kim JM, Gong G, Ryu JS, Kim WB, Yun SC, Shong YK. Prognostic parameters for recurrence of papillary thyroid microcarcinoma. BMC Cancer 2008; 8: 296
13 Noguchi S, Murakami N, Yamashita H, Toda M, Kawamoto H. Papillary thyroid carcinoma: modified radical neck dissection improves prognosis. Arch Surg 1998; 133: 276-280
14 Hay ID, Hutchinson ME, Gonzalez-Losada T, McIver B, Reinalda ME, Grant CS, Thompson GB, Sebo TJ, Goellner JR. Papillary thyroid microcarcinoma: a study of 900 cases observed in a 60-year period. Surgery 2008; 144: 980-987 discussion 987–988
15 Wada N, Duh Q, Sugino K, Iwasaki H, Kameyama K, Mimura T, Ito K, Takami H, Takanashi Y. 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
16 DeGroot LJ, Kaplan EL, McCormick M, Strauss FH. Natural history, treatment, and course of papillary thyroid carcinoma. J Clin Endocrinol Metab 1990; 71: 414-424
17 Cranshaw IM, Carnaille B. Micrometastases in thyroid cancer. An important finding?. Surg Oncol 2008; 17: 253-258
18 Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Pacini F, Schlumberger M, Sherman SI, Steward DL, Tuttle RM. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009; 19: 1167-1214
19 Jeon MJ, Yoon JH, Han JM, Yim JH, Hong SJ, Song DE, Ryu JS, Kim TY, Shong YK, Kim WB. The prognostic value of the metastatic lymph node ratio and maximal metastatic tumor size in pathologic N1a papillary thyroid carcinoma. Eur J Endocrinol 2013; 168: 219-225
20 Monchik JM, Simon CJ, Caragacianu DL, Thomay AA, Tsai V, Cohen J, Mazzaglia PJ. Does failure to perform prophylactic level VI node dissection leave persistent disease detectable by ultrasonography in patients with low-risk papillary carcinoma of the thyroid?. Surgery 2009; 146: 1182-1187
21 Rosenbaum MA, McHenry CR. Central neck dissection for papillary thyroid cancer. Arch Otolaryngol Head Neck Surg 2009; 135: 1092-1097
22 Mazzaferri E, Doherty G, Steward D. The pros and cons of prophylactic central compartment lymph node dissection for papillary thyroid carcinoma. Thyroid 2009; 19: 683-689
23 Hughes CJ, Shaha AR, Shah JP, Loree TR. Impact of lymph node metastasis in differentiated carcinoma of the thyroid: a matched-pair analysis. Head Neck 1996; 18: 127-132
24 Cady B, Sedgwick CE, Meissner WA, Wool MS, Salzman FA, Werber J. Risk factor analysis in differentiated thyroid cancer. Cancer 1979; 43: 810-820
25 Clark OH. Thyroid Cancer and lymph node metastases. J Surg Oncol 2012; 103: 615-618
26 Lundgren CI, Hall P, Dickman PW, Zedenius J. Clinically significant prognostic factors for differentiated thyroid carcinoma: a population-based, nested case-control study. Cancer 2006; 106: 524-531
27 Yu X, Wan Y, Sippel RS, Chen H. Should All Papillary Thyroid Microcarcinomas Be Aggressively Treated? An Analysis of 18,445 Cases. Ann Surg 2011; 254: 653-660
28 Gupta S, Ajise O, Dultz L, Wang B, Nonaka D, Ogilvie J, Heller KS, Patel KN. Follicular variant of papillary thyroid cancer: encapsulated, nonencapsulated, and diffuse: distinct biologic and clinical entities. Arch Otolaryngol Head Neck Surg 2012; 138: 227-233
29 Bai Y, Kakudo K, Li Y, Liu Z, Ozaki T, Ito Y, Kihara M, Miyauchi A. Subclassification of non-solid-type papillary thyroid carcinoma identification of high-risk group in common type. Cancer Sci 2008; 99: 1908-1915
30 Sawka AM, Brierley JD, Tsang RW, Thabane L, Rotstein L, Gafni A, Straus S, Goldstein DP. An updated systematic review and commentary examining the effectiveness of radioactive iodine remnant ablation in well-differentiated thyroid cancer. Endocrinol Metab Clin North Am 2008; 37: 457-480
31 Schmidt D, Szikszai A, Linke R, Bautz W, Kuwert T. Impact of 131I SPECT/spiral CT on nodal staging of differentiated thyroid carcinoma at the first radioablation. J Nucl Med 2009; 50: 18-23