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

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Abstract

The aim of the present study was to evaluate the clinical implications of the vascular index (VI) as a predicting factor for central and lateral lymph node metastasis (LNM) in patients with papillary thyroid microcarcinoma (PTMC). From January 2011 to October 2011, 588 patients (495 females, 93 males) who were diagnosed with PTMC were included. Clinicopathologic characteristics of patients and ultrasound (US) features of the lesions including VI were evaluated retrospectively. The VI was measured with QLAB 7.0 quantification software using preoperative Doppler US images. Univariate and multivariate analysis were used to assess predictive factors of LNM. From 588 patients, 140 patients (23.8 %) had central LNM and 26 patients (4.4 %) had lateral LNM on pathologic results. The presence of lateral LNM [odds ratio (OR) 5.46; 95 % confidence interval (CI) = 2.19–13.64], bilaterality (OR 2.16; 95 % CI 1.17–4.01), and increased tumor size (OR 1.15; 95 % CI 1.04–1.28) were significant independent factors for predicting central LNM. The presence of central LNM (OR 5.58; 95 % CI 2.22–14.04), upper third location of malignancy (OR 2.50; 95 % CI 1.01–6.21), and tumor size (OR 1.34; 95 % CI 1.03–1.73) were significant independent factors for predicting lateral LNM. However, the VI was not a significant predicting factor for both central and lateral LNM. Therefore, the VI of PTMC may not be useful for predicting central and lateral LNM in patients with PTMC.

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References

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  2. M.D. Bramley, B.J. Harrison, Papillary microcarcinoma of the thyroid gland. Br. J. Surg. 83(12), 1674–1683 (1996)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. J. Folkman, The role of angiogenesis in tumor growth. Semin. Cancer Biol. 3(2), 65–71 (1992)

    CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  19. S. Rehman, G.C. Jayson, Molecular imaging of antiangiogenic agents. Oncologist 10(2), 92–103 (2005)

    Article  CAS  PubMed  Google Scholar 

  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)

    CAS  PubMed  Google Scholar 

  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)

    CAS  PubMed  Google Scholar 

  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)

    PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    PubMed  Google Scholar 

  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)

    PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  38. E.L. Mazzaferri, Managing thyroid microcarcinomas. Yonsei Med. J. 53(1), 1–14 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  41. J.A. Goddard, D.L. Steward, Prophylactic central lymph node dissection in differentiated thyroid cancer. Endocrine 44(2), 275–277 (2013)

    Article  CAS  PubMed  Google Scholar 

  42. L. Wartofsky, D. Van Nostrand, Radioiodine treatment of well-differentiated thyroid cancer. Endocrine 42(3), 506–513 (2012)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  PubMed Central  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

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Shin, H.J., Kim, EK., Moon, H.J. et al. Can increased tumoral vascularity be a quantitative predicting factor of lymph node metastasis in papillary thyroid microcarcinoma?. Endocrine 47, 273–282 (2014). https://doi.org/10.1007/s12020-013-0131-8

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