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Assessment of Tumor-infiltrating Lymphocytes Predicts the Behavior of Early-stage Oral Tongue Cancer

Heikkinen, Ilkka DDS*,†; Bello, Ibrahim O. DDS, PhD*,‡; Wahab, Awais DDS*,†; Hagström, Jaana DDS, PhD*,§; Haglund, Caj MD, PhD§,∥; Coletta, Ricardo D. DDS, PhD; Nieminen, Pentti MSc, PhD#; Mäkitie, Antti A. MD, PhD**,††,‡‡; Salo, Tuula DDS, PhD*,†,§§; Leivo, Ilmo MD, PhD∥∥; Almangush, Alhadi DDS, PhD*,††,∥∥,¶¶

The American Journal of Surgical Pathology: October 2019 - Volume 43 - Issue 10 - p 1392–1396
doi: 10.1097/PAS.0000000000001323
Original Articles

Tumor-infiltrating lymphocytes (TILs) have shown a promising prognostic value in many epithelial cancers. We sought to assess the prognostic value of TILs in a multicenter cohort of early oral tongue squamous cell carcinoma (OTSCC). The percentage of TILs was assessed on the surgical resection slides stained with hematoxylin and eosin. The assessment of TILs was performed in the stromal compartment and in the intraepithelial compartment (at the invasive front and at the center of the tumor). We followed the method that was described recently by the International Immuno-Oncology Biomarker Working Group for the assessment of TILs. A total of 308 cases from the 5 Finnish university hospitals and from A.C. Camargo Cancer Center, São Paulo, Brazil, were included. We found a promising prognostic value for stromal TILs at the invasive front in the multivariable analysis with a hazard ratio of 2.61 (95% confidence interval [CI], 1.77-3.83; P<0.001) for overall survival, 1.99 (95% CI, 1.07-3.69; P=0.040) for disease-specific survival, and 1.94 (95% CI, 1.14-3.29; P=0.020) for disease-free survival. In conclusion, evaluation of TILs is simple and can aid in identifying the high-risk cases of early OTSCC. The method introduced by the International Immuno-Oncology Biomarker Working Group can be used for standardized determination of TILs in early OTSCC.

Departments of * Pathology

Oral and Maxillofacial Diseases

§Research Programs Unit, Translational Cancer Biology

††Research Programme in Systems Oncology, Faculty of Medicine, University of Helsinki

Departments of Surgery

**Otorhinolaryngology—Head and Neck Surgery, University of Helsinki and Helsinki University Hospital

#Medical Informatics and Data Analysis Research Group, University of Oulu

§§Cancer and Translational Medicine Research Unit, Medical Research Center Oulu, University of Oulu and Oulu University Hospital, Oulu

∥∥Institute of Biomedicine, Pathology, University of Turku, Turku, Finland

Department of Oral Medicine and Diagnostic Sciences, King Saud University College of Dentistry, Riyadh, Saudi Arabia

Department of Oral Diagnosis, School of Dentistry, University of Campinas, Piracicaba, São Paulo, Brazil

‡‡Department of Clinical Sciences, Intervention and Technology, Division of Ear, Nose and Throat Diseases, Karolinska Institute and Karolinska University Hospital, Stockholm, Sweden

¶¶Institute of Dentistry, University of Misurata, Misurata, Libya

T.S., I.L., and A.A. contributed equally.

Conflicts of Interest and Source of Funding: This study was funded by Turku University Hospital Fund, Helsinki University Hospital Research Fund, the Finnish Dental Society, the Rauha Ahokas Foundation, K. Albin Johanssons Foundation, the Sigrid Juselius Foundation, the Finnish Cancer Society, Finska Läkaresällskapet, and the Maritza and Reino Salonen Foundation. The authors have disclosed that they have no significant relationships with, or financial interest in, any commercial companies pertaining to this article.

Correspondence: Alhadi Almangush, DDS, PhD, Department of Pathology, University of Helsinki, Haartmaninkatu 3 (P.O. Box 21), Helsinki FIN-00014, Finland (e-mails:;

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