Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-17T20:21:36.375Z Has data issue: false hasContentIssue false

Tumour–node–metastasis staging of human papillomavirus negative upper aerodigestive tract cancers: a critical appraisal

Published online by Cambridge University Press:  08 October 2015

U Aydil*
Affiliation:
Department of Otorhinolaryngology, Head & Neck Surgery, Gazi University School of Medicine, Ankara, Turkey
U Duvvuri
Affiliation:
Department of Otorhinolaryngology, Head & Neck Surgery, University of Pittsburgh Medical Center, Pennsylvania, USA Section of Otolaryngology, Veterans Affairs Pittsburgh Health System, Pennsylvania, USA
Y Kizil
Affiliation:
Department of Otorhinolaryngology, Head & Neck Surgery, Gazi University School of Medicine, Ankara, Turkey
A Köybaşioğlu
Affiliation:
Department of Otorhinolaryngology, Head & Neck Surgery, Memorial Ankara Hospital, Turkey
*
Address for correspondence: Dr U Aydil, Gazi Üniversitesi Tıp Fakültesi KBB AD, 06500 Beşevler, Ankara, Turkey Fax: +90 312 202 4357 E-mail: utkuaydil@yahoo.com

Abstract

Objective:

The tumour–node–metastasis staging system has a dynamic structure that is continuously being updated as scientific data develops. This review discusses some suggested revisions on tumour–node–metastasis staging of human papillomavirus negative upper aerodigestive tract cancers.

Methods:

The seventh edition of The American Joint Committee on Cancer Staging Manual was reviewed and important issues that could be considered for revision were identified and discussed.

Results:

According to our assessment of the oncological outcomes of previous studies, the following factors should be considered for revision: anterior commissure involvement and subglottic extension in laryngeal cancers; underlying bone involvement in hard palate and upper alveolar ridge cancers; tumour thickness in oral cancers; and extracapsular spread and carotid artery involvement in neck metastases.

Conclusion:

Sufficient data on the prognostic importance of these issues have been reported. Suggested revisions in line with current knowledge on the clinical behaviour of upper aerodigestive tract cancers would improve the relevancy of staging.

Type
Review Articles
Copyright
Copyright © JLO (1984) Limited 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Edge, SB, Byrd, DR, Compton, CC, Fritz, AG, Greene, FL, Trotti, A, eds. AJCC Cancer Staging Manual, 7th edn.New York: Springer, 2010:5767Google ScholarPubMed
2Sobin, LH. TNM: evolution and relation to other prognostic factors. Semin Surg Oncol 2003;21:37CrossRefGoogle ScholarPubMed
3Ferlito, A, Rinaldo, A. The future of the TNM staging system in laryngeal cancer: time for a debate? Eur Arch Otorhinolaryngol 2008;265:1441–3CrossRefGoogle ScholarPubMed
4Takes, RP, Rinaldo, A, Silver, CE, Piccirillo, JF, Haigentz, M Jr, Suárez, C et al. Future of the TNM classification and staging system in head and neck cancer. Head Neck 2010;32:1693–711CrossRefGoogle ScholarPubMed
5Shah, J. Concerning the editorial “The future of the TNM staging system in laryngeal cancer: time for a debate?” by Ferlito and Rinaldo. Eur Arch Otorhinolaryngol 2009;266:155; author reply 157–8CrossRefGoogle ScholarPubMed
6Yoo, J, Lacchetti, C, Hammond, JA, Gilbert, RW; Head and Neck Cancer Disease Site Group. Role of endolaryngeal surgery (with or without laser) compared with radiotherapy in the management of early (T1) glottic cancer: a clinical practice guideline. Curr Oncol 2013;20:e132–5CrossRefGoogle Scholar
7Hartl, DM, Ferlito, A, Brasnu, DF, Langendijk, JA, Rinaldo, A, Silver, CE et al. Evidence-based review of treatment options for patients with glottic cancer. Head Neck 2011;33:1638–48CrossRefGoogle ScholarPubMed
8Aydil, U, Akmansu, M, Kizil, Y, Yazici, O, Ustün, S, Karaloğlu, F et al. An individualised treatment algorithm for tumour stage 1 glottic squamous cell carcinoma. J Laryngol Otol 2013;127:1127–33CrossRefGoogle ScholarPubMed
9Peretti, G, Piazza, C, Cocco, D, De Benedetto, L, Del Bon, F, Redaelli De Zinis, LO et al. Transoral CO(2) laser treatment for T(is)–T(3) glottic cancer: the University of Brescia experience on 595 patients. Head Neck 2010;32:977–83CrossRefGoogle Scholar
10Tong, CC, Au, KH, Ngan, RK, Chow, SM, Cheung, FY, Fu, YT et al. Impact and relationship of anterior commissure and time-dose factor on the local control of T1N0 glottic cancer treated by 6 MV photons. Radiat Oncol 2011;6:53CrossRefGoogle ScholarPubMed
11Rosier, JF, Grégoire, V, Counoy, H, Octave-Prignot, M, Rombaut, P, Scalliet, P et al. Comparison of external radiotherapy, laser microsurgery and partial laryngectomy for the treatment of T1N0M0 glottic carcinomas: a retrospective evaluation. Radiother Oncol 1998;48:175–83CrossRefGoogle ScholarPubMed
12Reddy, SP, Mohideen, N, Marra, S, Marks, JE. Effect of tumor bulk on local control and survival of patients with T1 glottic cancer. Radiother Oncol 1997;47:161–6CrossRefGoogle Scholar
13Hartl, DM, Landry, G, Bidault, F, Hans, S, Julieron, M, Mamelle, G et al. CT-scan prediction of thyroid cartilage invasion for early laryngeal squamous cell carcinoma. Eur Arch Otorhinolaryngol 2013;270:287–91CrossRefGoogle ScholarPubMed
14Agrawal, N, Ha, PK. Management of early-stage laryngeal cancer. Otolaryngol Clin North Am 2008;41:757–69CrossRefGoogle ScholarPubMed
15Rifai, M, Khattab, H. Anterior commissure carcinoma: I-histopathologic study. Am J Otolaryngol 2000;21:294–7CrossRefGoogle ScholarPubMed
16Spector, JG, Sessions, DG, Chao, KS, Haughey, BH, Hanson, JM, Simpson, JR et al. Stage I (T1 N0 M0) squamous cell carcinoma of the laryngeal glottis: therapeutic results and voice preservation. Head Neck 1999;21:707–173.0.CO;2-2>CrossRefGoogle Scholar
17Bradley, PJ, Rinaldo, A, Suárez, C, Shaha, AR, Leemans, CR, Langendijk, JA et al. Primary treatment of the anterior vocal commissure squamous carcinoma. Eur Arch Otorhinolaryngol 2006;263:879–88CrossRefGoogle ScholarPubMed
18Rucci, L, Gammarota, L, Borghi Cirri, MB. Carcinoma of the anterior commissure of the larynx: I. Embryological and anatomic considerations. Ann Otol Rhinol Laryngol 1996;105:303–8Google ScholarPubMed
19Rucci, L, Bocciolini, C, Romagnoli, P, Olofsson, J. Risk factors and prognosis of anterior commissure versus posterior commissure T1-T2 glottic cancer. Ann Otol Rhinol Laryngol 2003;112:223–9CrossRefGoogle ScholarPubMed
20Rifai, M, Heiba, MH, Salah, H. Anterior commissure carcinoma II: the role of salvage supracricoid laryngectomy. Am J Otolaryngol 2002;23:13CrossRefGoogle ScholarPubMed
21Steiner, W, Ambrosch, P, Rödel, RM, Kron, M. Impact of anterior commissure involvement on local control of early glottic carcinoma treated by laser microresection. Laryngoscope 2004;114:1485–91CrossRefGoogle ScholarPubMed
22Nozaki, M, Furuta, M, Murakami, Y, Izawa, Y, Iwasaki, N, Takahashi, H et al. Radiation therapy for T1 glottic cancer: involvement of the anterior commissure. Anticancer Res 2000;20:1121–4Google ScholarPubMed
23Bradley, PJ, Mackenzie, K, Wight, R, Pracy, P, Paleri, V; ENT-UK Head & Neck Group. Consensus statement on management in the UK: transoral laser assisted microsurgical resection of early glottic cancer. Clin Otolaryngol 2009;34:367–73CrossRefGoogle ScholarPubMed
24Remacle, M, Van Haverbeke, C, Eckel, H, Bradley, P, Chevalier, D, Djukic, V et al. Proposal for revision of the European Laryngological Society classification of endoscopic cordectomies. Eur Arch Otorhinolaryngol 2007;264:499504CrossRefGoogle ScholarPubMed
25Sachse, F, Stoll, W, Rudack, C. Evaluation of treatment results with regard to initial anterior commissure involvement in early glottic carcinoma treated by external partial surgery or transoral laser microresection. Head Neck 2009;31:531–7CrossRefGoogle ScholarPubMed
26Laccourreye, O, Weinstein, G, Brasnu, D, Trotoux, J, Laccourreye, H. Vertical partial laryngectomy: a critical analysis of local recurrence. Ann Otol Rhinol Laryngol 1991;100:6871CrossRefGoogle ScholarPubMed
27Chone, CT, Yonehara, E, Martins, JE, Altemani, A, Crespo, AN. Importance of anterior commissure in recurrence of early glottic cancer after laser endoscopic resection. Arch Otolaryngol Head Neck Surg 2007;133:882–7CrossRefGoogle ScholarPubMed
28Pradhan, SA, Pai, PS, Neeli, SI, D'Cruz, AK. Transoral laser surgery for early glottic cancers. Arch Otolaryngol Head Neck Surg 2003;129:623–5CrossRefGoogle ScholarPubMed
29Rödel, RM, Steiner, W, Müller, RM, Kron, M, Matthias, C. Endoscopic laser surgery of early glottic cancer: involvement of the anterior commissure. Head Neck 2009;31:583–92CrossRefGoogle ScholarPubMed
30Hakeem, AH, Tubachi, J, Pradhan, SA. Significance of anterior commissure involvement in early glottic squamous cell carcinoma treated with trans-oral CO2 laser microsurgery. Laryngoscope 2013;123:1912–17CrossRefGoogle ScholarPubMed
31Ferri, E, Armato, E. Diode laser microsurgery for treatment of Tis and T1 glottic carcinomas. Am J Otolaryngol 2008;29:101–5CrossRefGoogle ScholarPubMed
32Peretti, G, Nicolai, P, Redaelli De Zinis, LO, Berlucchi, M, Bazzana, T et al. Endoscopic CO2 laser excision for tis, T1, and T2 glottic carcinomas: cure rate and prognostic factors. Otolaryngol Head Neck Surg 2000;123:124–31CrossRefGoogle ScholarPubMed
33Ledda, GP, Puxeddu, R. Carbon dioxide laser microsurgery for early glottic carcinoma. Otolaryngol Head Neck Surg 2006;134:911–15CrossRefGoogle ScholarPubMed
34Rucci, L, Romagnoli, P, Scala, J. CO(2) laser therapy in Tis and T1 glottic cancer: indications and results. Head Neck 2010;32:392–8CrossRefGoogle ScholarPubMed
35Zouhair, A, Azria, D, Coucke, P, Matzinger, O, Bron, L, Moeckli, R et al. Decreased local control following radiation therapy alone in early-stage glottic carcinoma with anterior commissure extension. Strahlenther Onkol 2004;180:8490CrossRefGoogle ScholarPubMed
36Cellai, E, Frata, P, Magrini, SM, Paiar, F, Barca, R, Fondelli, S et al. Radical radiotherapy for early glottic cancer: results in a series of 1087 patients from two Italian radiation oncology centers. I. The case of T1N0 disease. Int J Radiat Oncol Biol Phys 2005;63:1378–86CrossRefGoogle Scholar
37Jin, J, Liao, Z, Gao, L, Huang, X, Xu, G. Analysis of prognostic factors for T(1)N(0)M(0) glottic cancer treated with definitive radiotherapy alone: experience of the cancer hospital of Peking Union Medical College and the Chinese Academy Of Medical Sciences. Int J Radiat Oncol Biol Phys 2002;54:471–8CrossRefGoogle Scholar
38Marshak, G, Brenner, B, Shvero, J, Shapira, J, Ophir, D, Hochman, I et al. Prognostic factors for local control of early glottic cancer: the Rabin Medical Center retrospective study on 207 patients. Int J Radiat Oncol Biol Phys 1999;43:1009–13CrossRefGoogle ScholarPubMed
39Smee, RI, Meagher, NS, Williams, JR, Broadley, K, Bridger, GP. Role of radiotherapy in early glottic carcinoma. Head Neck 2010;32:850–9CrossRefGoogle ScholarPubMed
40Laskar, SG, Baijal, G, Murthy, V, Chilukuri, S, Budrukkar, A, Gupta, T et al. Hypofractionated radiotherapy for T1N0M0 glottic cancer: retrospective analysis of two different cohorts of dose-fractionation schedules from a single institution. Clin Oncol (R Coll Radiol) 2012;24:e180–6CrossRefGoogle ScholarPubMed
41Khan, MK, Koyfman, SA, Hunter, GK, Reddy, CA, Saxton, JP. Definitive radiotherapy for early (T1–T2) glottic squamous cell carcinoma: a 20 year Cleveland Clinic experience. Radiat Oncol 2012;7:193CrossRefGoogle ScholarPubMed
42Hermans, R, Van den Bogaert, W, Rijnders, A, Baert, AL. Value of computed tomography as outcome predictor of supraglottic squamous cell carcinoma treated by definitive radiation therapy. Int J Radiat Oncol Biol Phys 1999;44:755–65CrossRefGoogle ScholarPubMed
43Burke, LS, Greven, KM, McGuirt, WT, Case, D, Hoen, HM, Raben, M. Definitive radiotherapy for early glottic carcinoma: prognostic factors and implications for treatment. Int J Radiat Oncol Biol Phys 1997;38:1001–6CrossRefGoogle ScholarPubMed
44Murakami, R, Nishimura, R, Baba, Y, Furusawa, M, Ogata, N, Yumoto, E et al. Prognostic factors of glottic carcinomas treated with radiation therapy: value of the adjacent sign on radiological examinations in the sixth edition of the UICC TNM staging system. Int J Radiat Oncol Biol Phys 2005;61:471–5CrossRefGoogle ScholarPubMed
45Mendenhall, WM, Amdur, RJ, Morris, CG, Hinerman, RW. T1–T2N0 squamous cell carcinoma of the glottic larynx treated with radiation therapy. J Clin Oncol 2001;19:4029–36CrossRefGoogle ScholarPubMed
46Dahm, JD, Sessions, DG, Paniello, RC, Harvey, J. Primary subglottic cancer. Laryngoscope 1998;108:741–6CrossRefGoogle ScholarPubMed
47Garas, J, McGuirt, WF Sr.Squamous cell carcinoma of the subglottis. Am J Otolaryngol 2006;27:14CrossRefGoogle ScholarPubMed
48Smee, RI, Williams, JR, Bridger, GP. The management dilemmas of invasive subglottic carcinoma. Clin Oncol (R Coll Radiol) 2008;20:751–6CrossRefGoogle ScholarPubMed
49Dadas, B, Uslu, B, Cakir, B, Ozdoğan, HC, Caliş, AB, Turgut, S. Intraoperative management of the thyroid gland in laryngeal cancer surgery. J Otolaryngol 2001;30:179–83CrossRefGoogle ScholarPubMed
50Paisley, S, Warde, PR, O'Sullivan, B, Waldron, J, Gullane, PJ, Payne, D et al. Results of radiotherapy for primary subglottic squamous cell carcinoma. Int J Radiat Oncol Biol Phys 2002;52:1245–50CrossRefGoogle ScholarPubMed
51Hata, M, Taguchi, T, Koike, I, Nishimura, G, Takahashi, M, Komatsu, M et al. Efficacy and toxicity of (chemo)radiotherapy for primary subglottic cancer. Strahlenther Onkol 2013;189:2632CrossRefGoogle ScholarPubMed
52Dagan, R, Morris, CG, Bennett, JA, Mancuso, AA, Amdur, RJ, Hinerman, RW et al. Prognostic significance of paraglottic space invasion in T2N0 glottic carcinoma. Am J Clin Oncol 2007;30:186–90CrossRefGoogle ScholarPubMed
53Garden, AS, Forster, K, Wong, PF, Morrison, WH, Schechter, NR, Ang, KK. Results of radiotherapy for T2N0 glottic carcinoma: does the “2” stand for twice-daily treatment? Int J Radiat Oncol Biol Phys 2003;55:322–8CrossRefGoogle ScholarPubMed
54Chen, MF, Chang, JT, Tsang, NM, Liao, CT, Chen, WC. Radiotherapy of early-stage glottic cancer: analysis of factors affecting prognosis. Ann Otol Rhinol Laryngol 2003;112:904–11CrossRefGoogle ScholarPubMed
55Mortuaire, G, Francois, J, Wiel, E, Chevalier, D. Local recurrence after CO2 laser cordectomy for early glottic carcinoma. Laryngoscope 2006;116:101–5CrossRefGoogle ScholarPubMed
56Mendelson, AA, Al-Khatib, TA, Julien, M, Payne, RJ, Black, MJ, Hier, MP. Thyroid gland management in total laryngectomy: meta-analysis and surgical recommendations. Otolaryngol Head Neck Surg 2009;140:298305CrossRefGoogle ScholarPubMed
57Medina, JE, Ferlito, A, Robbins, KT, Silver, CE, Rodrigo, JP, de Bree, R et al. Central compartment dissection in laryngeal cancer. Head Neck 2011;33:746–52CrossRefGoogle ScholarPubMed
58Rubin, J, Johnson, JT, Myers, EN. Stomal recurrence after laryngectomy: interrelated risk factor study. Otolaryngol Head Neck Surg 1990;103:805–12CrossRefGoogle ScholarPubMed
59Mantravadi, R, Katz, AM, Skolnik, EM, Becker, S, Freehling, DJ, Friedman, M. Stomal recurrence. A critical analysis of risk factors. Arch Otolaryngol 1981;107:735–8CrossRefGoogle ScholarPubMed
60Oztürkcan, S, Calli, C, Dündar, R, Tuna, B, Katilmiş, H, Aslan, H et al. Stomal recurrence after total laryngectomy: clinical and pathological analysis of risk factors [in Turkish]. Kulak Burun Bogaz Ihtis Derg 2009;19:146–50Google ScholarPubMed
61Ampil, F, Ghali, G, Caldito, G, Baluna, R. Post-laryngectomy stomal cancer recurrences, re-treatment decisions and outcomes: case series. J Craniomaxillofac Surg 2009;37:349–51CrossRefGoogle ScholarPubMed
62Yuen, AP, Wei, WI, Ho, WK, Hui, Y. Risk factors of tracheostomal recurrence after laryngectomy for laryngeal carcinoma. Am J Surg 1996;172:263–6CrossRefGoogle ScholarPubMed
63Reddy, SP, Narayana, A, Melian, E, Kathuria, S, Leman, C, Emami, B. Stomal recurrence in patients with T1 glottic cancer after salvage laryngectomy for radiotherapy failures: role of p53 overexpression and subglottic extension. Am J Clin Oncol 2001;24:124–7CrossRefGoogle ScholarPubMed
64Aydil, U, Kızıl, Y, Bakkal, FK, Köybaşıoğlu, A, Uslu, S. Neoplasms of the hard palate. J Oral Maxillofac Surg 2014;72:619–26CrossRefGoogle ScholarPubMed
65Mourouzis, C, Pratt, C, Brennan, PA. Squamous cell carcinoma of the maxillary gingiva, alveolus, and hard palate: is there a need for elective neck dissection? Br J Oral Maxillofac Surg 2010;48:345–8CrossRefGoogle Scholar
66Beltramini, GA, Massarelli, O, Demarchi, M, Copelli, C, Cassoni, A, Valentini, V et al. Is neck dissection needed in squamous-cell carcinoma of the maxillary gingiva, alveolus, and hard palate? A multicentre Italian study of 65 cases and literature review. Oral Oncol 2012;48:97101CrossRefGoogle ScholarPubMed
67Brown, JS, Bekiroglu, F, Shaw, RJ, Woolgar, JA, Rogers, SN. Management of the neck and regional recurrence in squamous cell carcinoma of the maxillary alveolus and hard palate compared with other sites in the oral cavity. Head Neck 2013;35:265–9CrossRefGoogle ScholarPubMed
68Ogura, I, Kurabayashi, T, Sasaki, T, Amagasa, T, Okada, N, Kaneda, T. Maxillary bone invasion by gingival carcinoma as an indicator of cervical metastasis. Dentomaxillofac Radiol 2003;32:291–4CrossRefGoogle ScholarPubMed
69Morris, LG, Patel, SG, Shah, JP, Ganly, I. High rates of regional failure in squamous cell carcinoma of the hard palate and maxillary alveolus. Head Neck 2011;33:824–30CrossRefGoogle ScholarPubMed
70Eskander, A, Givi, B, Gullane, PJ, Irish, J, Brown, D, Gilbert, RW et al. Outcome predictors in squamous cell carcinoma of the maxillary alveolus and hard palate. Laryngoscope 2013;123:2453–8CrossRefGoogle ScholarPubMed
71Hubert Low, TH, Gao, K, Elliott, M, Clark, JR. Tumor classification for early oral cancer: re-evaluate the current TNM classification. Head Neck 2015;37:223–8CrossRefGoogle ScholarPubMed
72Po Wing Yuen, A, Lam, KY, Lam, LK, Ho, CM, Wong, A, Chow, TL et al. Prognostic factors of clinically stage I and II oral tongue carcinoma-A comparative study of stage, thickness, shape, growth pattern, invasive front malignancy grading, Martinez-Gimeno score, and pathologic features. Head Neck 2002;24:513–20CrossRefGoogle Scholar
73Yuen, AP, Lam, KY, Wei, WI, Lam, KY, Ho, CM, Chow, TL et al. A comparison of the prognostic significance of tumor diameter, length, width, thickness, area, volume, and clinicopathological features of oral tongue carcinoma. Am J Surg 2000;180:139–43CrossRefGoogle ScholarPubMed
74Liao, CT, Lin, CY, Fan, KH, Wang, HM, Ng, SH, Lee, LY et al. Identification of a high-risk group among patients with oral cavity squamous cell carcinoma and pT1–2N0 disease. Int J Radiat Oncol Biol Phys 2012;82:284–90CrossRefGoogle ScholarPubMed
75Gonzalez-Moles, MA, Esteban, F, Rodriguez-Archilla, A, Ruiz-Avila, I, Gonzalez-Moles, S. Importance of tumour thickness measurement in prognosis of tongue cancer. Oral Oncol 2002;38:394–7CrossRefGoogle ScholarPubMed
76Huang, SH, Hwang, D, Lockwood, G, Goldstein, DP, O'Sullivan, B. Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies. Cancer 2009;115:1489–97CrossRefGoogle ScholarPubMed
77Freeman, SB, Hamaker, RC, Borrowdale, RW, Huntley, TC. Management of neck metastasis with carotid artery involvement. The management of the carotid artery, intraoperative radiation, survival, and complications are reviewed in 58 patients who underwent resection of their carotid arteries over a 13-year period. Laryngoscope 2004;114:20–4CrossRefGoogle Scholar
78Roh, JL, Kim, MR, Choi, SH, Lee, JH, Cho, KJ, Nam, SY et al. Can patients with head and neck cancers invading carotid artery gain survival benefit from surgery? Acta Otolaryngol 2008;128:1370–4CrossRefGoogle ScholarPubMed
79Zhengang, X, Colbert, S, Brennan, PA, Xue, B, Yongfa, Q, Pingzhang, T et al. Surgical management of metastases that involve the carotid artery in cases of primary squamous cell carcinoma of the head and neck. Int J Oral Maxillofac Surg 2013;42:440–5CrossRefGoogle ScholarPubMed
80Ozer, E, Agrawal, A, Ozer, HG, Schuller, DE, The Impact of Surgery in the Management of the Head and Neck Carcinoma Involving the Carotid Artery. Laryngoscope 2008;118:1771–4CrossRefGoogle ScholarPubMed
81Manzoor, NF, Russell, JO, Bricker, A, Koyfman, S, Scharpf, J, Burkey, B et al. Impact of surgical resection on survival in patients with advanced head and neck cancer involving the carotid artery. JAMA Otolaryngol Head Neck Surg 2013;139:1219–25CrossRefGoogle ScholarPubMed
82Meleca, RJ, Marks, SC. Carotid artery resection for cancer of the head and neck. Arch Otolaryngol Head Neck Surg 1994;120:974–8CrossRefGoogle ScholarPubMed
83Biller, HF, Urken, M, Lawson, W, Haimov, M. Carotid artery resection and bypass for neck carcinoma. Laryngoscope 1988;98:181–3CrossRefGoogle ScholarPubMed
84Freeman, SB. Advanced cervical metastasis involving the carotid artery. Curr Opin Otolaryngol Head Neck Surg 2005;13:107–11CrossRefGoogle ScholarPubMed
85Pons, Y, Ukkola-Pons, E, Clément, P, Gauthier, J, Conessa, C. Relevance of 5 different imaging signs in the evaluation of carotid artery invasion by cervical lymphadenopathy in head and neck squamous cell carcinoma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;109:775–8CrossRefGoogle ScholarPubMed
86Cooper, JS, Pajak, TF, Forastiere, AA, Jacobs, J, Campbell, BH, Saxman, SB et al. ; Radiation Therapy Oncology Group 9501/Intergroup. Postoperative concurrent radiotherapy and chemotherapy for high-risk squamous-cell carcinoma of the head and neck. N Engl J Med 2004;350:1937–44CrossRefGoogle ScholarPubMed
87Bernier, J, Domenge, C, Ozsahin, M, Matuszewska, K, Lefèbvre, JL, Greiner, RH et al. ; European Organization for Research and Treatment of Cancer Trial 22931. Postoperative irradiation with or without concomitant chemotherapy for locally advanced head and neck cancer. N Engl J Med 2004;350:1945–52CrossRefGoogle ScholarPubMed
88Puri, SK, Fan, CY, Hanna, E. Significance of extracapsular lymph node metastases in patients with head and neck squamous cell carcinoma. Curr Opin Otolaryngol Head Neck Surg 2003;11:119–23CrossRefGoogle ScholarPubMed
89Ferlito, A, Rinaldo, A, Devaney, KO, MacLennan, K, Myers, JN, Petruzzelli, GJ et al. Prognostic significance of microscopic and macroscopic extracapsular spread from metastatic tumor in the cervical lymph nodes. Oral Oncol 2002;38:747–51CrossRefGoogle ScholarPubMed
90de Juan, J, García, J, López, M, Orús, C, Esteller, E, Quer, M et al. Inclusion of extracapsular spread in the pTNM classification system: a proposal for patients with head and neck carcinoma. JAMA Otolaryngol Head Neck Surg 2013;139:483–8CrossRefGoogle ScholarPubMed
91Myers, JN, Greenberg, JS, Mo, V, Roberts, D. Extracapsular spread. A significant predictor of treatment failure in patients with squamous cell carcinoma of the tongue. Cancer 2001;92:3030–63.0.CO;2-P>CrossRefGoogle ScholarPubMed
92Oosterkamp, S, de Jong, JM, Van den Ende, PL, Manni, JJ, Dehing-Oberije, C, Kremer, B. Predictive value of lymph node metastases and extracapsular extension for the risk of distant metastases in laryngeal carcinoma. Laryngoscope 2006;116:2067–70CrossRefGoogle ScholarPubMed
93Greenberg, JS, Fowler, R, Gomez, J, Mo, V, Roberts, D, El Naggar, AK et al. Extent of extracapsular spread: a critical prognosticator in oral tongue cancer. Cancer 2003;97:1464–70CrossRefGoogle ScholarPubMed
94Shaw, RJ, Lowe, D, Woolgar, JA, Brown, JS, Vaughan, ED, Evans, C et al. Extracapsular spread in oral squamous cell carcinoma. Head Neck 2010;32:714–22CrossRefGoogle ScholarPubMed
95Jose, J, Coatesworth, AP, Johnston, C, MacLennan, K. Cervical node metastases in squamous cell carcinoma of the upper aerodigestive tract: the significance of extracapsular spread and soft tissue deposits. Head Neck 2003;25:451–6CrossRefGoogle ScholarPubMed
96Alvi, A, Johnson, JT. Extracapsular spread in the clinically negative neck (N0): implications and outcome. Otolaryngol Head Neck Surg 1996;114:6570CrossRefGoogle ScholarPubMed
97Ghadjar, P, Simcock, M, Schreiber-Facklam, H, Zimmer, Y, Gräter, R, Evers, C et al. Incidence of small lymph node metastases with evidence of extracapsular extension: clinical implications in patients with head and neck squamous cell carcinoma. Int J Radiat Oncol Biol Phys 2010;78:1366–72CrossRefGoogle ScholarPubMed
98Apisarnthanarax, S, Elliott, DD, El-Naggar, AK, Asper, JA, Blanco, A, Ang, KK et al. Determining optimal clinical target volume margins in head-and-neck cancer based on microscopic extracapsular extension of metastatic neck nodes. Int J Radiat Oncol Biol Phys 2006;64:678–83CrossRefGoogle ScholarPubMed
99Sinha, P, Lewis, JS Jr, Piccirillo, JF, Kallogjeri, D, Haughey, BH. Extracapsular spread and adjuvant therapy in human papillomavirus-related, p16-positive oropharyngeal carcinoma. Cancer 2012;118:3519–30CrossRefGoogle ScholarPubMed
100Maxwell, JH, Ferris, RL, Gooding, W, Cunningham, D, Mehta, V, Kim, S et al. Extracapsular spread in head and neck carcinoma: impact of site and human papillomavirus status. Cancer 2013;119:3302–8CrossRefGoogle ScholarPubMed
101Gospodarowicz, MK, Miller, D, Groome, PA, Greene, FL, Logan, PA, Sobin, LH. The process for continuous improvement of the TNM classification. Cancer 2004;100:15CrossRefGoogle ScholarPubMed