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01-07-2015 | Original Article

For early-stage oral tongue cancer, depth of invasion and worst pattern of invasion are the strongest pathological predictors for locoregional recurrence and mortality

Authors: Alhadi Almangush, Ibrahim O. Bello, Ricardo D. Coletta, Antti A. Mäkitie, Laura K. Mäkinen, Joonas H. Kauppila, Matti Pukkila, Jaana Hagström, Jussi Laranne, Ylermi Soini, Veli-Matti Kosma, Petri Koivunen, Natalie Kelner, Luiz Paulo Kowalski, Reidar Grénman, Ilmo Leivo, Esa Läärä, Tuula Salo

Published in: Virchows Archiv | Issue 1/2015

Abstract

Despite early diagnosis and treatment, almost 20 % of patients with early-stage (cT1-cT2N0) oral tongue squamous cell carcinoma (OTSCC) still die of their disease. The prognosis of OTSCC patients is influenced by several demographic, clinical, and histopathologic factors. The aim of this multicenter international study was to find which of the factors age, gender, stage, grade, lymphocytic host response, perineural invasion, worst pattern of invasion, or depth of invasion has the strongest prognostic power in early-stage OTSCC. Patient data of 479 patients with early-stage (cT1-2N0) OTSCC in Finland, Brazil, and the USA were retrieved and analyzed using Cox proportional hazards regression models. Our results indicate that depth of invasion (DOI) and worst pattern of invasion (WPOI) are the strongest pathological predictors for locoregional recurrence, with a hazard ratio (HR) for 4 mm DOI of 1.67 (95 % confidence interval (CI) 1.07–2.60) and HR for WPOI of 1.46 (95 % CI 0.95–2.25). In addition, mortality from early OTSCC was also predicted by DOI (HR 2.44, 95 % CI 1.34–4.47) and by WPOI (HR 2.34, 95 % CI 1.26–4.32). We suggest that clinically early-stage oral tongue carcinomas 4 mm or deeper, or with a growth pattern of small cell islands or satellites, should be considered as high-risk tumors which require multimodality treatment.

Rusthoven K, Ballonoff A, Raben D, Chen C (2008) Poor prognosis in patients with stage I and II oral tongue squamous cell carcinoma. Cancer 112:345–351PubMedCrossRef

Myers JN, Elkins T, Roberts D, Byers RM (2000) Squamous cell carcinoma of the tongue in young adults: increasing incidence and factors that predict treatment outcomes. Otolaryngol Head Neck Surg 122:44–51PubMedCrossRef

Annertz K, Anderson H, Biorklund A, Moller T, Kantola S, Mork J, Olsen JH, Wennerberg J (2002) Incidence and survival of squamous cell carcinoma of the tongue in Scandinavia, with special reference to young adults. Int J Cancer 101:95–99PubMedCrossRef

Shiboski CH, Schmidt BL, Jordan RC (2005) Tongue and tonsil carcinoma: increasing trends in the U.S. population ages 20–44 years. Cancer 103:1843–1849PubMedCrossRef

Sopka DM, Li T, Lango MN, Mehra R, Liu JC, Burtness B, Flieder DB, Ridge JA, Galloway TJ (2013) Dysplasia at the margin? Investigating the case for subsequent therapy in ‘low-risk’ squamous cell carcinoma of the oral tongue. Oral Oncol 49:1083–1087PubMedCentralPubMedCrossRef

Dunkel J, Vaittinen S, Grenman R, Kinnunen I, Irjala H (2013) Prognostic markers in stage I oral cavity squamous cell carcinoma. Laryngoscope 123:2435–2441PubMed

Thomas B, Stedman M, Davies L (2014) Grade as a prognostic factor in oral squamous cell carcinoma: a population-based analysis of the data. Laryngoscope 124:688–694PubMedCrossRef

Shim SJ, Cha J, Koom WS, Kim GE, Lee CG, Choi EC, Keum KC (2010) Clinical outcomes for T1-2N0-1 oral tongue cancer patients underwent surgery with and without postoperative radiotherapy. Radiat Oncol 5:43PubMedCentralPubMedCrossRef

Sharma P, Shah SV, Taneja C, Patel AM, Patel MD (2013) A prospective study of prognostic factors for recurrence in early oral tongue cancer. J Clin Diagn Res 7:2559–2562PubMedCentralPubMed

10.

Chatzistamou I, Rodriguez J, Jouffroy T, Girod A, Point D, Sklavounou A, Kittas C, Sastre-Garau X, Klijanienko J (2010) Prognostic significance of tumor shape and stromal chronic inflammatory infiltration in squamous cell carcinomas of the oral tongue. J Oral Pathol Med 39:667–671PubMedCrossRef

11.

Lundqvist L, Stenlund H, Laurell G, Nylander K (2012) The importance of stromal inflammation in squamous cell carcinoma of the tongue. J Oral Pathol Med 41:379–383PubMedCrossRef

12.

Rodrigues PC, Miguel MC, Bagordakis E, Fonseca FP, de Aquino SN, Santos-Silva AR, Lopes MA, Graner E, Salo T, Kowalski LP, Coletta RD (2014) Clinicopathological prognostic factors of oral tongue squamous cell carcinoma: a retrospective study of 202 cases. Int J Oral Maxillofac Surg 43:795–801PubMedCrossRef

13.

Almangush A, Bello IO, Keski-Santti H, Makinen LK, Kauppila JH, Pukkila M, Hagstrom J, Laranne J, Tommola S, Nieminen O, Soini Y, Kosma VM, Koivunen P, Grenman R, Leivo I, Salo T (2014) Depth of invasion, tumor budding, and worst pattern of invasion: prognostic indicators in early-stage oral tongue cancer. Head Neck 36:811–818PubMedCentralPubMedCrossRef

14.

Chen YW, Yu EH, Wu TH, Lo WL, Li WY, Kao SY (2008) Histopathological factors affecting nodal metastasis in tongue cancer: analysis of 94 patients in Taiwan. Int J Oral Maxillofac Surg 37:912–916PubMedCrossRef

15.

Chatzistefanou I, Lubek J, Markou K, Ord RA (2014) The role of neck dissection and postoperative adjuvant radiotherapy in cN0 patients with PNI-positive squamous cell carcinoma of the oral cavity. Oral Oncol 50:753–758PubMedCrossRef

16.

Brandwein-Gensler M, Teixeira MS, Lewis CM, Lee B, Rolnitzky L, Hille JJ, Genden E, Urken ML, Wang BY (2005) Oral squamous cell carcinoma: histologic risk assessment, but not margin status, is strongly predictive of local disease-free and overall survival. Am J Surg Pathol 29:167–178PubMedCrossRef

17.

Li Y, Bai S, Carroll W, Dayan D, Dort JC, Heller K, Jour G, Lau H, Penner C, Prystowsky M, Rosenthal E, Schlecht NF, Smith RV, Urken M, Vered M, Wang B, Wenig B, Negassa A, Brandwein-Gensler M (2013) Validation of the risk model: high-risk classification and tumor pattern of invasion predict outcome for patients with low-stage oral cavity squamous cell carcinoma. Head Neck Pathol 7:211–223PubMedCentralPubMedCrossRef

18.

Oc P, Pillai G, Patel S, Fisher C, Archer D, Eccles S, Rhys-Evans P (2003) Tumour thickness predicts cervical nodal metastases and survival in early oral tongue cancer. Oral Oncol 39:386–390CrossRef

19.

Ganly I, Goldstein D, Carlson DL, Patel SG, O’Sullivan B, Lee N, Gullane P, Shah JP (2013) Long-term regional control and survival in patients with “low-risk,” early stage oral tongue cancer managed by partial glossectomy and neck dissection without postoperative radiation: the importance of tumor thickness. Cancer 119:1168–1176PubMedCrossRef

20.

Lin MJ, Guiney A, Iseli CE, Buchanan M, Iseli TA (2011) Prophylactic neck dissection in early oral tongue squamous cell carcinoma 2.1 to 4.0 mm depth. Otolaryngol Head Neck Surg 144:542–548PubMedCrossRef

21.

Huang SH, Hwang D, Lockwood G, Goldstein DP, O’Sullivan B (2009) 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 115:1489–1497PubMedCrossRef

22.

Hubert Low TH, Gao K, Elliott M, Clark JR (2015) Tumor classification for early oral cancer: re-evaluate the current TNM classification. Head Neck 37:223–228PubMedCrossRef

23.

Ebrahimi A, Gil Z, Amit M, Yen TC, Liao CT, Chaturvedi P, Agarwal JP, Kowalski LP, Kreppel M, Cernea CR, Brandao J, Bachar G, Bolzoni Villaret A, Fliss D, Fridman E, Robbins KT, Shah JP, Patel SG, Clark JR (2014) Primary tumor staging for oral cancer and a proposed modification incorporating depth of invasion: an international multicenter retrospective study. JAMA Otolaryngol Head Neck Surg 140:1138–1148PubMedCrossRef

24.

Kelner N, Rodrigues PC, Bufalino A, Fonseca FP, Dos Santos-Silva AR, Miguel MC, Pinto CA, Leme AF, Graner E, Salo T, Kowalski LP, Coletta RD (2014) Activin A immunoexpression as predictor of occult lymph node metastasis and overall survival in oral tongue squamous cell carcinoma. Head Neck. doi:10.1002/hed.23627 PubMed

25.

Chang AM, Kim SW, Duvvuri U, Johnson JT, Myers EN, Ferris RL, Gooding WE, Seethala RR, Chiosea SI (2013) Early squamous cell carcinoma of the oral tongue: comparing margins obtained from the glossectomy specimen to margins from the tumor bed. Oral Oncol 49:1077–1082PubMedCrossRef

26.

Jerjes W, Upile T, Petrie A, Riskalla A, Hamdoon Z, Vourvachis M, Karavidas K, Jay A, Sandison A, Thomas GJ, Kalavrezos N, Hopper C (2010) Clinicopathological parameters, recurrence, locoregional and distant metastasis in 115 T1-T2 oral squamous cell carcinoma patients. Head Neck Oncol 2:9PubMedCentralPubMedCrossRef

27.

Brandwein-Gensler M, Smith RV, Wang B, Penner C, Theilken A, Broughel D, Schiff B, Owen RP, Smith J, Sarta C, Hebert T, Nason R, Ramer M, DeLacure M, Hirsch D, Myssiorek D, Heller K, Prystowsky M, Schlecht NF, Negassa A (2010) Validation of the histologic risk model in a new cohort of patients with head and neck squamous cell carcinoma. Am J Surg Pathol 34:676–688PubMed

28.

Garavello W, Spreafico R, Gaini RM (2007) Oral tongue cancer in young patients: a matched analysis. Oral Oncol 43:894–897PubMedCrossRef

29.

Garavello W, Spreafico R, Somigliana E, Gaini L, Pignataro L, Gaini RM (2008) Prognostic influence of gender in patients with oral tongue cancer. Otolaryngol Head Neck Surg 138:768–771PubMedCrossRef

30.

Girod A, Mosseri V, Jouffroy T, Point D, Rodriguez J (2009) Women and squamous cell carcinomas of the oral cavity and oropharynx: is there something new? J Oral Maxillofac Surg 67:1914–1920PubMedCrossRef

31.

Goldenberg D, Brooksby C, Hollenbeak CS (2009) Age as a determinant of outcomes for patients with oral cancer. Oral Oncol 45:e57–e61PubMedCrossRef

32.

Chang TS, Chang CM, Ho HC, Su YC, Chen LF, Chou P, Lee CC (2013) Impact of young age on the prognosis for oral cancer: a population-based study in Taiwan. PLoS One 8:e75855PubMedCentralPubMedCrossRef

33.

Soudry E, Preis M, Hod R, Hamzany Y, Hadar T, Bahar G, Strenov Y, Shpitzer T (2010) Squamous cell carcinoma of the oral tongue in patients younger than 30 years: clinicopathologic features and outcome. Clin Otolaryngol 35:307–312PubMedCrossRef

34.

Hilly O, Shkedy Y, Hod R, Soudry E, Mizrachi A, Hamzany Y, Bachar G, Shpitzer T (2013) Carcinoma of the oral tongue in patients younger than 30 years: comparison with patients older than 60 years. Oral Oncol 49:987–990PubMedCrossRef

35.

Fang QG, Shi S, Liu FY, Sun CF (2014) Tongue squamous cell carcinoma as a possible distinct entity in patients under 40 years old. Oncol Lett 7:2099–2102PubMedCentralPubMed

36.

Mark Taylor S, Drover C, Maceachern R, Bullock M, Hart R, Psooy B, Trites J (2010) Is preoperative ultrasonography accurate in measuring tumor thickness and predicting the incidence of cervical metastasis in oral cancer? Oral Oncol 46:38–41PubMedCrossRef

37.

Lodder WL, Teertstra HJ, Tan IB, Pameijer FA, Smeele LE, van Velthuysen ML, van den Brekel MW (2011) Tumour thickness in oral cancer using an intra-oral ultrasound probe. Eur Radiol 21:98–106PubMedCentralPubMedCrossRef

38.

Iwai H, Kyomoto R, Ha-Kawa SK, Lee S, Yamashita T (2002) Magnetic resonance determination of tumor thickness as predictive factor of cervical metastasis in oral tongue carcinoma. Laryngoscope 112:457–461PubMedCrossRef

39.

Preda L, Chiesa F, Calabrese L, Latronico A, Bruschini R, Leon ME, Renne G, Bellomi M (2006) Relationship between histologic thickness of tongue carcinoma and thickness estimated from preoperative MRI. Eur Radiol 16:2242–2248PubMedCrossRef

40.

Okura M, Iida S, Aikawa T, Adachi T, Yoshimura N, Yamada T, Kogo M (2008) Tumor thickness and paralingual distance of coronal MR imaging predicts cervical node metastases in oral tongue carcinoma. AJNR Am J Neuroradiol 29:45–50PubMedCrossRef

41.

Jung J, Cho NH, Kim J, Choi EC, Lee SY, Byeon HK, Park YM, Yang WS, Kim SH (2009) Significant invasion depth of early oral tongue cancer originated from the lateral border to predict regional metastases and prognosis. Int J Oral Maxillofac Surg 38:653–660PubMedCrossRef

Title: For early-stage oral tongue cancer, depth of invasion and worst pattern of invasion are the strongest pathological predictors for locoregional recurrence and mortality
Authors: Alhadi Almangush
Ibrahim O. Bello
Ricardo D. Coletta
Antti A. Mäkitie
Laura K. Mäkinen
Joonas H. Kauppila
Matti Pukkila
Jaana Hagström
Jussi Laranne
Ylermi Soini
Veli-Matti Kosma
Petri Koivunen
Natalie Kelner
Luiz Paulo Kowalski
Reidar Grénman
Ilmo Leivo
Esa Läärä
Tuula Salo
Publication date: 01-07-2015
Publisher: Springer Berlin Heidelberg
Published in: Virchows Archiv / Issue 1/2015
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI: https://doi.org/10.1007/s00428-015-1758-z

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For early-stage oral tongue cancer, depth of invasion and worst pattern of invasion are the strongest pathological predictors for locoregional recurrence and mortality

Abstract

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Abstract

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