Can increased tumoral vascularity be a quantitative predicting factor of lymph node metastasis in papillary thyroid microcarcinoma?

Endocrine

Volumn 47, Issue 1, 2014, Pages 273-282

  Shin, Hyun Joo ^a   Kim, Eun Kyung ^a   Moon, Hee Jung ^a   Yoon, Jung Hyun ^a   Han, Kyung Hwa ^b   Kwak, Jin Young ^a  

^a Yonsei University College of Medicine   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

Papillary thyroid microcarcinoma; Thyroid; Ultrasound; Vascularity

Indexed keywords

ADULT; AGED; ARTICLE; BLOOD VESSEL PARAMETERS; CANCER STAGING; CLINICAL EVALUATION; CLINICAL FEATURE; DOPPLER ECHOGRAPHY; FEMALE; FINE NEEDLE ASPIRATION BIOPSY; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; PAPILLARY THYROID MICROCARCINOMA; PREDICTION; PREOPERATIVE EVALUATION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RETROSPECTIVE STUDY; THYROID PAPILLARY CARCINOMA; THYROIDECTOMY; TUMOR VASCULARIZATION; TUMOR VOLUME; VASCULAR INDEX; CARCINOMA; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; PROGNOSIS; THYROID NEOPLASMS; VASCULARIZATION; YOUNG ADULT;

ADULT; AGED; CARCINOMA; FEMALE; HUMANS; LYMPHATIC METASTASIS; MALE; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; PROGNOSIS; RETROSPECTIVE STUDIES; THYROID NEOPLASMS; THYROIDECTOMY; TUMOR BURDEN; YOUNG ADULT;

EID: 84906933859     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-013-0131-8     Document Type: Article

References (56)

1. H.R. Shin, K.W. Jung, Y.J. Won, J.G. Park, K.-A. Hospitals, 2002 Annual report of the Korea Central Cancer Registry: based on registered data from 139 hospitals. Cancer Res. Treat. 36(2), 103-114 (2004)
2. M.D. Bramley, B.J. Harrison, Papillary microcarcinoma of the thyroid gland. Br. J. Surg. 83(12), 1674-1683 (1996)
3. H.R. Harach, K.O. Franssila, V.M. Wasenius, Occult papillary carcinoma of the thyroid. A "normal" finding in Finland. A systematic autopsy study. Cancer 56(3), 531-538 (1985)
4. J.Y. Kwak, E.K. Kim, M.J. Kim, E.J. Son, W.Y. Chung, C.S. Park, K.H. Nam, Papillary microcarcinoma of the thyroid: predicting factors of lateral neck node metastasis. Ann. Surg. Oncol. 16(5), 1348-1355 (2009)
5. J.Y. Kwak, E.K. Kim, W.Y. Chung, H.J. Moon, M.J. Kim, J.R. Choi, Association of BRAFV600E mutation with poor clinical prognostic factors and US features in Korean patients with papillary thyroid microcarcinoma. Radiology 253(3), 854-860 (2009)
6. S.S. Kim, B.J. Lee, J.C. Lee, S.J. Kim, S.H. Lee, Y.K. Jeon, B.H. Kim, Y.K. Kim, I.J. Kim, Preoperative ultrasonographic tumor characteristics as a predictive factor of tumor stage in papillary thyroid carcinoma. Head Neck 33(12), 1719-1726 (2011)
7. J.S. Choi, J. Kim, J.Y. Kwak, M.J. Kim, H.S. Chang, E.K. Kim, Preoperative staging of papillary thyroid carcinoma: comparison of ultrasound imaging and CT. AJR Am. J. Roentgenol. 193(3), 871-878 (2009)
8. Y. Ito, C. Tomoda, T. Uruno, Y. Takamura, A. Miya, K. Kobayashi, F. Matsuzuka, K. Kuma, A. Miyauchi, Preoperative ultrasonographic examination for lymph node metastasis: usefulness when designing lymph node dissection for papillary microcarcinoma of the thyroid. World J. Surg. 28(5), 498-501 (2004)
9. S.S. Kim, B.J. Lee, J.C. Lee, S.H. Song, B.H. Kim, S.M. Son, I.J. Kim, Y.K. Kim, Y.H. Kang, Preoperative serum thyroid stimulating hormone levels in well-differentiated thyroid carcinoma is a predictive factor for lateral lymph node metastasis as well as extrathyroidal extension in Korean patients: a single-center experience. Endocrine 39(3), 259-265 (2011)
10. C. Eloy, J. Santos, P. Soares, M. Sobrinho-Simoes, Intratumoural lymph vessel density is related to presence of lymph node metastases and separates encapsulated from infiltrative papillary thyroid carcinoma. Virchows Arch. 459(6), 595-605 (2011)
11. J.Y. Kwak, E.K. Kim, M.J. Kim, S.H. Choi, E. Son, K.K. Oh, Power Doppler sonography: evaluation of solid breast lesions and correlation with lymph node metastasis. Clin. Imaging 32(3), 167-171 (2008)
12. K. Lee, J. Park do, G. Choe, H.H. Kim, W.H. Kim, H.S. Lee, Increased intratumoral lymphatic vessel density correlates with lymph node metastasis in early gastric carcinoma. Ann. Surg. Oncol. 17(1), 73-80 (2010)
13. J. Folkman, E. Merler, C. Abernathy, G. Williams, Isolation of a tumor factor responsible for angiogenesis. J. Exp. Med. 133(2), 275-288 (1971)
14. J. Folkman, The role of angiogenesis in tumor growth. Semin. Cancer Biol. 3(2), 65-71 (1992)
15. A. Sternberg, M. Amar, R. Alfici, G. Groisman, Conclusions from a study of venous invasion in stage IV colorectal adenocarcinoma. J. Clin. Pathol. 55(1), 17-21 (2002)
16. N. Lassau, M. Lamuraglia, S. Koscielny, A. Spatz, A. Roche, J. Leclere, M.F. Avril, Prognostic value of angiogenesis evaluated with high-frequency and colour Doppler sonography for preoperative assessment of primary cutaneous melanomas: correlation with recurrence after a 5 year follow-up period. Cancer Imaging 6, 24-29 (2006)
17. C.N. Chen, Y.M. Cheng, M.T. Lin, F.J. Hsieh, P.H. Lee, K.J. Chang, Association of color Doppler vascularity index and microvessel density with survival in patients with gastric cancer. Ann. Surg. 235(4), 512-518 (2002)
18. C.A. Cuenod, L. Fournier, D. Balvay, J.M. Guinebretiere, Tumor angiogenesis: pathophysiology and implications for contrast-enhanced MRI and CT assessment. Abdom. Imaging 31(2), 188-193 (2006)
19. S. Rehman, G.C. Jayson, Molecular imaging of antiangiogenic agents. Oncologist 10(2), 92-103 (2005)
20. Y. Takahashi, Y. Kitadai, C.D. Bucana, K.R. Cleary, L.M. Ellis, Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res. 55(18), 3964-3968 (1995)
21. N. Tanigawa, H. Amaya, M. Matsumura, T. Shimomatsuya, Correlation between expression of vascular endothelial growth factor and tumor vascularity, and patient outcome in human gastric carcinoma. J. Clin. Oncol. 15(2), 826-832 (1997)
22. W.W. Zhan, P. Zhou, J.Q. Zhou, S.Y. Xu, K.M. Chen, Differences in sonographic features of papillary thyroid carcinoma between neck lymph node metastatic and nonmetastatic groups. J. Ultrasound Med. 31(6), 915-920 (2012)
23. C.N. Chen, J.J. Lin, H. Lee, Y.M. Cheng, K.J. Chang, F.J. Hsieh, H.S. Lai, C.C. Chang, P.H. Lee, Association between color Doppler vascularity index, angiogenesis-related molecules, and clinical outcomes in gastric cancer. J. Surg. Oncol. 99(7), 402-408 (2009)
24. A.C. Fleischer, K.J. Niermann, E.F. Donnelly, T.E. Yankeelov, K.M. Canniff, D.E. Hallahan, M.E. Rothenberg, Sonographic depiction of microvessel perfusion: principles and potential. J. Ultrasound Med. 23(11), 1499-1506 (2004)
25. A. Lyshchik, R. Moses, S.L. Barnes, T. Higashi, R. Asato, M.I. Miga, J.C. Gore, A.C. Fleischer, Quantitative analysis of tumor vascularity in benign and malignant solid thyroid nodules. J. Ultrasound Med. 26(6), 837-846 (2007)
26. H.H. Chen, K.C. Lu, C.J. Lin, C.J. Wu, Role of the parathyroid gland vascularization index in predicting percutaneous ethanol injection efficacy in refractory uremic hyperparathyroidism. Nephron Clin Pract 117(2), c120-c126 (2011)
27. H.A. Pan, M.H. Wu, Y.C. Cheng, L.H. Wu, F.M. Chang, Quantification of ovarian stromal Doppler signals in poor responders undergoing in vitro fertilization with three-dimensional power Doppler ultrasonography. Am. J. Obstet. Gynecol. 190(2), 338-344 (2004)
28. E.K. Kim, C.S. Park, W.Y. Chung, K.K. Oh, D.I. Kim, J.T. Lee, H.S. Yoo, New sonographic criteria for recommending fine-needle aspiration biopsy of nonpalpable solid nodules of the thyroid. AJR Am. J. Roentgenol. 178(3), 687-691 (2002)
29. H.J. Moon, J.Y. Kwak, M.J. Kim, E.J. Son, E.K. Kim, Can vascularity at power Doppler US help predict thyroid malignancy? Radiology 255 (1), 260-269 (2010)
30. H.J. Moon, J.M. Sung, E.K. Kim, J.H. Yoon, J.H. Youk, J.Y. Kwak, Diagnostic performance of gray-scale US and elastography in solid thyroid nodules. Radiology 262(3), 1002-1013 (2012)
31. M.J. Lee, S.W. Hong, W.Y. Chung, J.Y. Kwak, M.J. Kim, E.K. Kim, Cytological results of ultrasound-guided fine-needle aspiration cytology for thyroid nodules: emphasis on correlation with sonographic findings. Yonsei Med. J. 52(5), 838-844 (2011)
32. H.J. Moon, E.K. Kim, W.Y. Chung, J.H. Yoon, J.Y. Kwak, Minimal extrathyroidal extension in patients with papillary thyroid microcarcinoma: is it a real prognostic factor? Ann. Surg. Oncol. 18(7), 1916-1923 (2011)
33. J.Y. Kwak, E.K. Kim, J.H. Youk, M.J. Kim, E.J. Son, S.H. Choi, K.K. Oh, Extrathyroid extension of well-differentiated papillary thyroid microcarcinoma on US. Thyroid 18(6), 609-614 (2008)
34. M. Ying, A. Ahuja, C. Metreweli, Diagnostic accuracy of sonographic criteria for evaluation of cervical lymphadenopathy. J. Ultrasound Med. 17(7), 437-445 (1998)
35. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, D.S. Cooper, G.M. Doherty, B.R. Haugen, R.T. Kloos, S.L. Lee, S.J. Mandel, E.L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S.I. Sherman, D.L. Steward, R.M. Tuttle, Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 19(11), 1167-1214 (2009)
36. D.W. Kim, S.J. Jeon, C.G. Kim, Usefulness of thyroglobulin measurement in needle washouts of fine-needle aspiration biopsy for the diagnosis of cervical lymph node metastases from papillary thyroid cancer before thyroidectomy. Endocrine 42(2), 399-403 (2012)
37. S.B. Edge, C.C. Compton, The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann. Surg. Oncol. 17(6), 1471-1474 (2010)
38. E.L. Mazzaferri, Managing thyroid microcarcinomas. Yonsei Med. J. 53(1), 1-14 (2012)
39. R. Gallicchio, S. Giacomobono, D. Capacchione, A. Nardelli, F. Barbato, A. Nappi, T. Pellegrino, G. Storto, Should patients with remnants from thyroid microcarcinoma really not be treated with iodine-131 ablation? Endocrine 44(2), 426-433 (2013)
40. G. Conzo, D. Pasquali, G. Bellastella, K. Esposito, C. Carella, A. De Bellis, G. Docimo, M. Klain, S. Iorio, S. Napolitano, A. Palazzo, A. Pizza, A.A. Sinisi, E. Zampella, A. Bellastella, L. Santini, Total thyroidectomy, without prophylactic central lymph node dissection, in the treatment of differentiated thyroid cancer. Clinical retrospective study on 221 cases. Endocrine 44(2), 419-425 (2013)
41. J.A. Goddard, D.L. Steward, Prophylactic central lymph node dissection in differentiated thyroid cancer. Endocrine 44(2), 275-277 (2013)
42. L. Wartofsky, D. Van Nostrand, Radioiodine treatment of well-differentiated thyroid cancer. Endocrine 42(3), 506-513 (2012)
43. D.S. Cooper, G.M. Doherty, B.R. Haugen, R.T. Kloos, S.L. Lee, S.J. Mandel, E.L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S.I. Sherman, D.L. Steward, R.M. Tuttle, Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 19(11), 1167-1214 (2009)
44. S. Bonnet, D. Hartl, S. Leboulleux, E. Baudin, J.D. Lumbroso, A. Al Ghuzlan, L. Chami, M. Schlumberger, J.P. Travagli, Prophylactic lymph node dissection for papillary thyroid cancer less than 2 cm: implications for radioiodine treatment. J. Clin. Endocrinol. Metab. 94 (4), 1162-1167 (2009)
45. D.J. Hicklin, L.M. Ellis, Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J. Clin. Oncol. 23(5), 1011-1027 (2005)
46. N. Weidner, J.P. Semple, W.R. Welch, J. Folkman, Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. N. Engl. J. Med. 324(1), 1-8 (1991)
47. Y. Choi, K.J. Park, S. Ryu, D.H. Kim, J. Yun, D.K. Kang, M. Chun, Papillary thyroid carcinoma involving cervical neck lymph nodes: correlations with lymphangiogenesis and ultrasound features. Endocr. J. 59(10), 941-948 (2012)
48. C.N. Chen, Y.M. Cheng, J.T. Liang, P.H. Lee, F.J. Hsieh, R.H. Yuan, S.M. Wang, M.F. Chang, K.J. Chang, Color Doppler vascularity index can predict distant metastasis and survival in colon cancer patients. Cancer Res. 60(11), 2892-2897 (2000)
49. E.L. Mazzaferri, R.L. Young, Papillary thyroid carcinoma: a 10 year follow-up report of the impact of therapy in 576 patients. Am. J. Med. 70(3), 511-518 (1981)
50. K.E. Kim, E.K. Kim, J.H. Yoon, K.H. Han, H.J. Moon, J.Y. Kwak, Preoperative prediction of central lymph node metastasis in thyroid papillary microcarcinoma using clinicopathologic and sonographic features. World J Surg 37(2), 385-391 (2013)
51. Y.S. Lim, J.C. Lee, Y.S. Lee, B.J. Lee, S.G. Wang, S.M. Son, I.J. Kim, Lateral cervical lymph node metastases from papillary thyroid carcinoma: predictive factors of nodal metastasis. Surgery 150(1), 116-121 (2011)
52. A. Machens, H.J. Holzhausen, H. Dralle, The prognostic value of primary tumor size in papillary and follicular thyroid carcinoma. Cancer 103(11), 2269-2273 (2005)
53. R. Katoh, J. Sasaki, H. Kurihara, K. Suzuki, Y. Iida, A. Kawaoi, Multiple thyroid involvement (intraglandular metastasis) in papillary thyroid carcinoma. A clinicopathologic study of 105 consecutive patients. Cancer 70 (6), 1585-1590 (1992)
54. Y. Ito, C. Tomoda, T. Uruno, Y. Takamura, A. Miya, K. Kobayashi, F. Matsuzuka, K. Kuma, A. Miyauchi, Papillary microcarcinoma of the thyroid: how should it be treated? World J. Surg. 28(11), 1115-1121 (2004)
55. O. Algin, E. Algin, G. Gokalp, G. Ocakoglu, C. Erdogan, O. Saraydaroglu, E. Tuncel, Role of duplex power Doppler ultrasound in differentiation between malignant and benign thyroid nodules. Korean J Radiol 11(6), 594-602 (2010)
56. S. Sancak, A. Hardt, R. Gartner, M. Eszlinger, A. Aslan, F.T. Eren, B.M. Gulluoglu, L.S. Sen, Z. Sever, N.S. Akalin, R. Paschke, Comparison of Color Flow Doppler Sonography (CFDS) and immunohistologic detection of microvessels for the assessment of the malignancy of thyroid nodules. Horm. Metab. Res. 42(9), 670-676 (2010)