Original Article
Papillary thyroid carcinoma nodal surgery directed by a preoperative radiographic map utilizing CT scan and ultrasound in all primary and reoperative patients
David Lesnik MD,
Mary Elizabeth Cunnane MD,
David Zurakowski PhD,
Gul Ozbilen Acar MD,
Cenk Ecevit MD,
Alasdair Mace MD,
Dipti Kamani MD,
Gregory W. Randolph MD,
David Lesnik MD
Division of Thyroid and Parathyroid Surgery, Massachusetts Eye and Ear Infirmary, Department of Otology and Laryngology, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorMary Elizabeth Cunnane MD
Department of Radiology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorDavid Zurakowski PhD
Departments of Anesthesiology and Surgery, Children's Hospital, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorGul Ozbilen Acar MD
Department of Otorhinolaryngology, Goztepe Research and Education Hospital, Istanbul, Turkey
Search for more papers by this authorCenk Ecevit MD
Department of Otorhinolaryngology, Goztepe Research and Education Hospital, Istanbul, Turkey
Search for more papers by this authorAlasdair Mace MD
Charing Cross Hospital and St. Mary's Hospital, Imperial College London, United Kingdom
Search for more papers by this authorDipti Kamani MD
Division of Thyroid and Parathyroid Surgery, Massachusetts Eye and Ear Infirmary, Department of Otology and Laryngology, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorCorresponding Author
Gregory W. Randolph MD
Division of Thyroid and Parathyroid Surgery, Massachusetts Eye and Ear Infirmary, Department of Otology and Laryngology, Harvard Medical School, Boston, Massachusetts
Division of Surgical Oncology, Endocrine Surgery Service, Department of Surgery, Massachusetts General Hospital, Boston, Massachusetts
243 Charles St., Boston, MA 02114. E-mail: [email protected]Search for more papers by this author
David Lesnik MD,
Mary Elizabeth Cunnane MD,
David Zurakowski PhD,
Gul Ozbilen Acar MD,
Cenk Ecevit MD,
Alasdair Mace MD,
Dipti Kamani MD,
Gregory W. Randolph MD,
David Lesnik MD
Division of Thyroid and Parathyroid Surgery, Massachusetts Eye and Ear Infirmary, Department of Otology and Laryngology, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorMary Elizabeth Cunnane MD
Department of Radiology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorDavid Zurakowski PhD
Departments of Anesthesiology and Surgery, Children's Hospital, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorGul Ozbilen Acar MD
Department of Otorhinolaryngology, Goztepe Research and Education Hospital, Istanbul, Turkey
Search for more papers by this authorCenk Ecevit MD
Department of Otorhinolaryngology, Goztepe Research and Education Hospital, Istanbul, Turkey
Search for more papers by this authorAlasdair Mace MD
Charing Cross Hospital and St. Mary's Hospital, Imperial College London, United Kingdom
Search for more papers by this authorDipti Kamani MD
Division of Thyroid and Parathyroid Surgery, Massachusetts Eye and Ear Infirmary, Department of Otology and Laryngology, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorCorresponding Author
Gregory W. Randolph MD
Division of Thyroid and Parathyroid Surgery, Massachusetts Eye and Ear Infirmary, Department of Otology and Laryngology, Harvard Medical School, Boston, Massachusetts
Division of Surgical Oncology, Endocrine Surgery Service, Department of Surgery, Massachusetts General Hospital, Boston, Massachusetts
243 Charles St., Boston, MA 02114. E-mail: [email protected]Search for more papers by this authorAbstract
Background
To study the diagnostic accuracy of physical examination (PE), ultrasonography (US), contrastenhanced computed tomography (CT) and in preoperative detection of macroscopic nodal metastasis in primary/recurrent papillary thyroid carcinoma (PTC) patients to determine if the routine addition of CT would be beneficial in accurate preoperative lymph-node surgery planning.
Methods
In a tertiary center prospective study, 162 PTC patients underwent preoperative lymph-node evaluation by PE, US, and CT. Sensitivity, specificity, positive/negative predictive value (PPV/NPV) of each nodal detection technique were calculated in central/lateral cervical compartments. The gold standard for diagnostic-accuracy was surgical pathology.
Results
In patients undergoing primary (Group I)/revision (Group II) surgical treatment for PTC, combined US/CT yielded significantly higher sensitivity for macroscopic lymph-node detection in both lateral and central neck, most marked in Group I-central compartment.
Conclusions
Combined preoperative US/CT provides reliable, objective, preoperative macroscopic nodal metastasis map to design rational nodal surgery in primary/revision PTC patients. © 2013 Wiley Periodicals, Inc. Head Neck 36: 191–202, 2014
REFERENCES
- 1Wang TS, Dubner S, Sznyter LA, Heller KS. Incidence of metastatic well-differentiated thyroid cancer in cervical lymph nodes. Arch Otolaryngol Head Neck Surg 2004; 130: 110–113.
- 2Noguchi M, Hashimoto T, Ohyama S, Tajiri K, Fujii H, Miyazaki I. Indications for bilateral neck dissection in well-differentiated carcinoma of the thyroid. Jpn J Surg 1987; 17: 439–444.
- 3Noguchi M, Yamada H, Ohta N, et al. Regional lymph node metastases in well-differentiated thyroid carcinoma. Int Surg 1987; 72: 100–103.
- 4Noguchi S, Murakami N. The value of lymph-node dissection in patients with differentiated thyroid cancer. Surg Clin North Am 1987; 67: 251–261.
- 5Mirallié E, Visset J, Sagan C, Hamy A, Le Bodic MF, Paineau J. Localization of cervical node metastasis of papillary thyroid carcinoma. World J Surg 1999; 23: 970–973; discussion 973–974.
- 6Qubain SW, Nakano S, Baba M, Takao S, Aikou T. Distribution of lymph node micrometastasis in pN0 well-differentiated thyroid carcinoma. Surgery 2002; 131: 249–256.
- 7Triponez F, Poder L, Zarnegar R, et al. Hook needle-guided excision of recurrent differentiated thyroid cancer in previously operated neck compartments: a safe technique for small, nonpalpable recurrent disease. J Clin Endocrinol Metab 2006; 91: 4943–4947.
- 8Ito Y, Higashiyama T, Takamura Y, et al. Risk factors for recurrence to the lymph node in papillary thyroid carcinoma patients without preoperatively detectable lateral node metastasis: validity of prophylactic modified radical neck dissection. World J Surg 2007; 31: 2085–2091.
- 9Lim YC, Choi EC, Yoon YH, Kim EH, Koo BS. Central lymph node metastases in unilateral papillary thyroid microcarcinoma. Br J Surg 2009; 96: 253–257.
- 10Lee SK, Choi JH, Lim HI, et al. Sentinel lymph node biopsy in papillary thyroid cancer: comparison study of blue dye method and combined radioisotope and blue dye method in papillary thyroid cancer. Eur J Surg Oncol 2009; 35: 974–979.
- 11Ross DS, Litofsky D, Ain KB, et al. Recurrence after treatment of micropapillary thyroid cancer. Thyroid 2009; 19: 1043–1048.
- 12Gemsenjäger E, Perren A, Seifert B, Schüler G, Schweizer I, Heitz PU. Lymph node surgery in papillary thyroid carcinoma. J Am Coll Surg 2003; 197: 182–190.
- 13Cranshaw IM, Carnaille B. Micrometastases in thyroid cancer. An important finding?Surg Oncol 2008; 17: 253–258.
- 14Bardet S, Malville E, Rame JP, et al. Macroscopic lymph-node involvement and neck dissection predict lymph-node recurrence in papillary thyroid carcinoma. Eur J Endocrinol 2008; 158: 551–560.
- 15Baudin E, Travagli JP, Ropers J, et al. Microcarcinoma of the thyroid gland: the Gustave–Roussy Institute experience. Cancer 1998; 83: 553–559.
10.1002/(SICI)1097-0142(19980801)83:3<553::AID-CNCR25>3.0.CO;2-U CASPubMedWeb of Science®Google Scholar
- 16Chow SM, Law SC, 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.
- 17Giordano D, Gradoni P, Oretti G, Molina E, Ferri T. Treatment and prognostic factors of papillary thyroid microcarcinoma. Clin Otolaryngol 2010; 35: 118–124.
- 18Hay ID. Management of patients with low-risk papillary thyroid carcinoma. Endocr Pract 2007; 13: 521–533.
- 19Hay 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: 980–987; discussion 987–988.
- 20Ito Y, Uruno T, Nakano K, et al. An observation trial without surgical treatment in patients with papillary microcarcinoma of the thyroid. Thyroid 2003; 13: 381–387.
- 21Mazzaferri EL. Management of low-risk differentiated thyroid cancer. Endocr Pract 2007; 13: 498–512.
- 22Noguchi S, Yamashita H, Uchino S, Watanabe S. Papillary microcarcinoma. World J Surg 2008; 32: 747–753.
- 23Roti E, Rossi R, Trasforini G, et al. Clinical and histological characteristics of papillary thyroid microcarcinoma: results of a retrospective study in 243 patients. J Clin Endocrinol Metab 2006; 91: 2171–2178.
- 24So YK, Son YI, Hong SD, et al. Subclinical lymph node metastasis in papillary thyroid microcarcinoma: a study of 551 resections. Surgery 2010; 148: 526–531.
- 25Wada 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.
- 26Yamashita H, Noguchi S, Murakami N, et al. Extracapsular invasion of lymph node metastasis. A good indicator of disease recurrence and poor prognosis in patients with thyroid microcarcinoma. Cancer 1999; 86: 842–849.
10.1002/(SICI)1097-0142(19990901)86:5<842::AID-CNCR21>3.0.CO;2-X CASPubMedWeb of Science®Google Scholar
- 27Zetoune T, Keutgen X, Buitrago D, et al. Prophylactic central neck dissection and local recurrence in papillary thyroid cancer: a meta-analysis. Ann Surg Oncol 2010; 17: 3287–3293.
- 28Randolph GW, Duh QY, Heller KS, et al. The prognostic significance of nodal metastases from papillary thyroid carcinoma can be stratified based on the size and number of metastatic lymph nodes, as well as the presence of extranodal extension. Thyroid 2012; 22: 1144–1152.
- 29Kouvaraki MA, Lee JE, Shapiro SE, Sherman SI, Evans DB. Preventable reoperations for persistent and recurrent papillary thyroid carcinoma. Surgery 2004; 136: 1183–1191.
- 30Bachelot A, Leboulleux S, Baudin E, et al. Neck recurrence from thyroid carcinoma: serum thyroglobulin and high-dose total body scan are not reliable criteria for cure after radioiodine treatment. Clin Endocrinol (Oxf) 2005; 62: 376–379.
- 31 American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer,Cooper DS, Doherty GM, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009; 19: 1167–1214.
- 32Choi JS, Kim J, Kwak JY, Kim MJ, Chang HS, Kim EK. Preoperative staging of papillary thyroid carcinoma: comparison of ultrasound imaging and CT. AJR Am J Roentgenol 2009; 193: 871–878.
- 33Takashima S, Sone S, Takayama F, et al. Papillary thyroid carcinoma: MR diagnosis of lymph node metastasis. AJNR Am J Neuroradiol 1998; 19: 509–513.
- 34Gross ND, Weissman JL, Talbot JM, Andersen PE, Wax MK, Cohen JI. MRI detection of cervical metastasis from differentiated thyroid carcinoma. Laryngoscope 2001; 111( 11 Pt 1): 1905–1909.
- 35Ito Y, Tomoda C, Uruno T, et al. Preoperative ultrasonographic examination for lymph node metastasis: usefulness when designing lymph node dissection for papillary microcarcinoma of the thyroid. World J Surg 2004; 28: 498–501.
- 36Kouvaraki MA, Shapiro SE, Fornage BD, et al. Role of preoperative ultrasonography in the surgical management of patients with thyroid cancer. Surgery 2003; 134: 946–954; discussion 954–955.
- 37Kaneko K, Abe K, Baba S, et al. Can calcification predict 131I accumulation on metastatic lymph nodes in papillary thyroid carcinoma patients receiving 131I therapy? Comparison of CT, 131I WBS and 18F-FDG PET/CT. Eur Radiol 2010; 20: 477–483.
- 38Park JS, Son KR, Na DG, Kim E, Kim S. 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 2009; 192: 66–72.
- 39Roh JL, Park JY, Kim JM, Song CJ. Use of preoperative ultrasonography as guidance for neck dissection in patients with papillary thyroid carcinoma. J Surg Oncol 2009; 99: 28–31.
- 40Ito Y, Tomoda C, Uruno T, et al. Ultrasonographically and anatomopathologically detectable node metastases in the lateral compartment as indicators of worse relapse-free survival in patients with papillary thyroid carcinoma. World J Surg 2005; 29: 917–920.
- 41Hwang HS, Orloff LA. Efficacy of preoperative neck ultrasound in the detection of cervical lymph node metastasis from thyroid cancer. Laryngoscope 2011; 121: 487–491.
- 42Machens A, Hinze R, Thomusch O, Dralle H. Pattern of nodal metastasis for primary and reoperative thyroid cancer. World J Surg 2002; 26: 22–28.
- 43Johnson NA, Tublin ME. Postoperative surveillance of differentiated thyroid carcinoma: rationale, techniques, and controversies. Radiology 2008; 249: 429–444.
- 44Rosário PW, de Faria S, Bicalho L, et al. Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J Ultrasound Med 2005; 24: 1385–1389.
- 45Kuna SK, Bracic I, Tesic V, Kuna K, Herceg GH, Dodig D. Ultrasonographic differentiation of benign from malignant neck lymphadenopathy in thyroid cancer. J Ultrasound Med 2006; 25: 1531–1537; quiz 1538–1540.
- 46Wunderbaldinger P, Harisinghani MG, Hahn PF, et al. Cystic lymph node metastases in papillary thyroid carcinoma. AJR Am J Roentgenol 2002; 178: 693–697.
- 47Stulak JM, Grant CS, Farley DR, et al. Value of preoperative ultrasonography in the surgical management of initial and reoperative papillary thyroid cancer. Arch Surg 2006; 141: 489–494; discussion 494–496.
- 48Ahn JE, Lee JH, Yi JS, et al. Diagnostic accuracy of CT and ultrasonography for evaluating metastatic cervical lymph nodes in patients with thyroid cancer. World J Surg 2008; 32: 1552–1558.
- 49Yoon DY, Hwang HS, Chang SK, et al. CT, MR, US, 18F-FDG PET/CT, and their combined use for the assessment of cervical lymph node metastases in squamous cell carcinoma of the head and neck. Eur Radiol 2009; 19: 634–642.
- 50 American Thyroid Association Surgery Working Group; American Association of Endocrine Surgeons; American Academy of Otolaryngology-Head and Neck Surgery, et al. Consensus statement on the terminology and classification of central neck dissection for thyroid cancer. Thyroid 2009; 19: 1153–1158.
- 51Koch GG, Landis JR, Freeman JL, Freeman DHJr, Lehnen RC. A general methodology for the analysis of experiments with repeated measurement of categorical data. Biometrics 1977; 33: 133–158.
- 52Newcombe RG. Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 1998; 17: 857–872.
10.1002/(SICI)1097-0258(19980430)17:8<857::AID-SIM777>3.0.CO;2-E CASPubMedWeb of Science®Google Scholar
- 53Price RM, Bonett DG. Confidence intervals for a ratio of two independent binomial proportions. Stat Med 2008; 27: 5497–5508.
- 54Vittinghoff E, Glidden DV, Shiboski SC, McCulloch CE. Regression methods in biostatistics. Linear, logistic, survival, and repeated measures models. Statistics for Biology and Health. 2nd Ed.New York:Springer;2005.
- 55Lundgren 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.
- 56Ito Y, Miyauchi A. A therapeutic strategy for incidentally detected papillary microcarcinoma of the thyroid. Nat Clin Pract Endocrinol Metab 2007; 3: 240–248.
- 57Lee X, Gao M, Ji Y, et al. Analysis of differential BRAF(V600E) mutational status in high aggressive papillary thyroid microcarcinoma. Ann Surg Oncol 2009; 16: 240–245.
- 58Lim DJ, Baek KH, Lee YS, et al. Clinical, histopathological, and molecular characteristics of papillary thyroid microcarcinoma. Thyroid 2007; 17: 883–888.
- 59Park YJ, Kim YA, Lee YJ, et al. Papillary microcarcinoma in comparison with larger papillary thyroid carcinoma in BRAF(V600E) mutation, clinicopathological features, and immunohistochemical findings. Head Neck 2010; 32: 38–45.
- 60Scheumann GF, Gimm O, Wegener G, Hundeshagen H, Dralle H. Prognostic significance and surgical management of locoregional lymph node metastases in papillary thyroid cancer. World J Surg 1994; 18: 559–567; discussion 567–568.
- 61Tisell LE, Nilsson B, Mölne J, et al. Improved survival of patients with papillary thyroid cancer after surgical microdissection. World J Surg 1996; 20: 854–859.
- 62Ito Y, Tomoda C, Uruno T, et al. Papillary microcarcinoma of the thyroid: how should it be treated?World J Surg 2004; 28: 1115–1121.
- 63Coburn MC, Wanebo HJ. Prognostic factors and management considerations in patients with cervical metastases of thyroid cancer. Am J Surg 1992; 164: 671–676.
- 64Hughes 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.
10.1002/(SICI)1097-0347(199603/04)18:2<127::AID-HED3>3.0.CO;2-3 CASPubMedWeb of Science®Google Scholar
- 65Sato N, Oyamatsu M, Koyama Y, Emura I, Tamiya Y, Hatakeyama K. Do the level of nodal disease according to the TNM classification and the number of involved cervical nodes reflect prognosis in patients with differentiated carcinoma of the thyroid gland?J Surg Oncol 1998; 69: 151–155.
- 66Loh KC, Greenspan FS, Dong F, Miller TR, Yeo PP. Influence of lymphocytic thyroiditis on the prognostic outcome of patients with papillary thyroid carcinoma. J Clin Endocrinol Metab 1999; 84: 458–463.
- 67Mazzaferri EL, Jhiang SM. Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med 1994; 97: 418–428.
- 68Cady B, Rossi R. An expanded view of risk-group definition in differentiated thyroid carcinoma. Surgery 1988; 104: 947–953.
- 69Leboulleux 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: 3590–3594.
- 70Hay ID, Grant CS, Taylor WF, McConahey WM. Ipsilateral lobectomy versus bilateral lobar resection in papillary thyroid carcinoma: a retrospective analysis of surgical outcome using a novel prognostic scoring system. Surgery 1987; 102: 1088–1095.
- 71Cady B, Sedgwick CE, Meissner WA, Wool MS, Salzman FA, Werber J. Risk factor analysis in differentiated thyroid cancer. Cancer 1979; 43: 810–820.
10.1002/1097-0142(197903)43:3<810::AID-CNCR2820430306>3.0.CO;2-B CASPubMedWeb of Science®Google Scholar
- 72Ito 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: 91–99.
- 73Ito Y, Jikuzono T, Higashiyama T, et al. Clinical significance of lymph node metastasis of thyroid papillary carcinoma located in one lobe. World J Surg 2006; 30: 1821–1828.
- 74Podnos YD, Smith D, Wagman LD, Ellenhorn JD. The implication of lymph node metastasis on survival in patients with well-differentiated thyroid cancer. Am Surg 2005; 71: 731–734.
- 75Shindo M, Wu JC, Park EE, Tanzella F. The importance of central compartment elective lymph node excision in the staging and treatment of papillary thyroid cancer. Arch Otolaryngol Head Neck Surg 2006; 132: 650–654.
- 76Ito Y, Miyauchi A, Inoue H, et al. An observational trial for papillary thyroid microcarcinoma in Japanese patients. World J Surg 2010; 34: 28–35.
- 77Sugitani I, Toda K, Yamada K, Yamamoto N, Ikenaga M, Fujimoto Y. Three distinctly different kinds of papillary thyroid microcarcinoma should be recognized: our treatment strategies and outcomes. World J Surg 2010; 34: 1222–1231.
- 78White ML, Gauger PG, Doherty GM. Central lymph node dissection in differentiated thyroid cancer. World J Surg 2007; 31: 895–904.
- 79Pereira JA, Jimeno J, Miquel J, et al. Nodal yield, morbidity, and recurrence after central neck dissection for papillary thyroid carcinoma. Surgery 2005; 138: 1095–1100; discussion 1100–1101.
- 80Sywak M, Cornford L, Roach P, Stalberg P, Sidhu S, Delbridge L. Routine ipsilateral level VI lymphadenectomy reduces postoperative thyroglobulin levels in papillary thyroid cancer. Surgery 2006; 140: 1000–1005; discussion 1005–1007.
- 81Wada N, Masudo K, Nakayama H, et al. Clinical outcomes in older or younger patients with papillary thyroid carcinoma: impact of lymphadenopathy and patient age. Eur J Surg Oncol 2008; 34: 202–207.
- 82Moley JF, DeBenedetti MK. Patterns of nodal metastases in palpable medullary thyroid carcinoma: recommendations for extent of node dissection. Ann Surg 1999; 229: 880–887; discussion 887–888.
- 83Golder WA. Lymph node diagnosis in oncologic imaging: a dilemma still waiting to be solved. Onkologie 2004; 27: 194–199.
- 84Ahuja A, Ying M. Grey-scale sonography in assessment of cervical lymphadenopathy: review of sonographic appearances and features that may help a beginner. Br J Oral Maxillofac Surg 2000; 38: 451–459.
- 85Loevner LA. Imaging of the thyroid gland. Semin Ultrasound CT MR 1996; 17: 539–562.
- 86Sipos JA. Advances in ultrasound for the diagnosis and management of thyroid cancer. Thyroid 2009; 19: 1363–1372.
- 87Kim E, Park JS, Son KR, Kim JH, Jeon SJ, Na DG. Preoperative diagnosis of cervical metastatic lymph nodes in papillary thyroid carcinoma: comparison of ultrasound, computed tomography, and combined ultrasound with computed tomography. Thyroid 2008; 18: 411–418.
- 88King AD, Tse GM, Ahuja AT, et al. Necrosis in metastatic neck nodes: diagnostic accuracy of CT, MR imaging, and US. Radiology 2004; 230: 720–726.
- 89Sarvanan K, Bapuraj JR, Sharma SC, Radotra BD, Khandelwal N, Suri S. Computed tomography and ultrasonographic evaluation of metastatic cervical lymph nodes with surgicoclinicopathologic correlation. J Laryngol Otol 2002; 116: 194–199.
- 90Rodgers SE, Hunter GJ, Hamberg LM, et al. Improved preoperative planning for directed parathyroidectomy with 4-dimensional computed tomography. Surgery 2006; 140: 932–940; discussion 940–941.
- 91Nygaard B, Nygaard T, Jensen LI, et al. Iohexol: effects on uptake of radioactive iodine in the thyroid and on thyroid function. Acad Radiol 1998; 5: 409–414.
- 92Thomsen HS; European Society of Urogenital Radiology. European Society of Urogenital Radiology guidelines on contrast media application. Curr Opin Urol 2007; 17: 70–76.
- 93Lundgren CI, Hall P, Dickman PW, Zedenius J. Influence of surgical and postoperative treatment on survival in differentiated thyroid cancer. Br J Surg 2007; 94: 571–577.
- 94Pacini F, Schlumberger M, Dralle H, et al. European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. Eur J Endocrinol 2006; 154: 787–803.
- 95Tala Jury HP, Castagna MG, Fioravanti C, Cipri C, Brianzoni E, Pacini F. Lack of association between urinary iodine excretion and successful thyroid ablation in thyroid cancer patients. J Clin Endocrinol Metab 2010; 95: 230–237.
- 96Podnos YD, Smith DD, Wagman LD, Ellenhorn JD. Survival in patients with papillary thyroid cancer is not affected by the use of radioactive isotope. J Surg Oncol 2007; 96: 3–7.
- 97Smith–Bindman R, Lipson J, Marcus R, et al. Radiation dose associated with common computed tomography examinations and the associated lifetime attributable risk of cancer. Arch Intern Med 2009; 169: 2078–2086.
