Tertiary lymphoid structures associate with improved survival in early oral tongue cancer

Alhadi Almangush; Ibrahim O Bello; Amr Elseragy; Jaana Hagström; Caj Haglund; Luiz Paulo Kowalski; Pentti Nieminen; Ricardo D Coletta; Antti A Mäkitie; Tuula Salo; Ilmo Leivo

doi:10.1186/s12885-022-10208-z

Tertiary lymphoid structures associate with improved survival in early oral tongue cancer

BMC Cancer. 2022 Oct 30;22(1):1108. doi: 10.1186/s12885-022-10208-z.

Authors

Alhadi Almangush^{1

2

3

4}, Ibrahim O Bello^#^{5

6}, Amr Elseragy^#^{7

8}, Jaana Hagström^{5

9

10}, Caj Haglund^{11

12}, Luiz Paulo Kowalski¹³, Pentti Nieminen¹⁴, Ricardo D Coletta¹⁵, Antti A Mäkitie^{16

17

18}, Tuula Salo^#^{5

8}, Ilmo Leivo^#^{19

20}

Affiliations

¹ Department of Pathology, University of Helsinki, Haartmaninkatu 3, P.O. Box 21, Helsinki, N00014, Finland. alhadi.almangush@helsinki.fi.
² Faculty of Medicine, Research Program in Systems Oncology, University of Helsinki, Helsinki, Finland. alhadi.almangush@helsinki.fi.
³ Institute of Biomedicine, Pathology, University of Turku, Turku, Finland. alhadi.almangush@helsinki.fi.
⁴ Faculty of Dentistry, Misurata University, Misurata, Libya. alhadi.almangush@helsinki.fi.
⁵ Department of Pathology, University of Helsinki, Haartmaninkatu 3, P.O. Box 21, Helsinki, N00014, Finland.
⁶ Department of Oral Medicine and Diagnostic Sciences, King Saud University College of Dentistry, Riyadh, Saudi Arabia.
⁷ Cancer and Translational Medicine Research Unit, University of Oulu, 90014, Oulu, Finland.
⁸ Department of Oral and Maxillofacial Diseases, University of Helsinki, Helsinki, Finland.
⁹ Research Programs Unit, Translational Cancer Medicine, University of Helsinki, Helsinki, Finland.
¹⁰ Department of Oral Pathology and Radiology, University of Turku, Turku, Finland.
¹¹ Research Programs Unit, Translational Cancer Medicine, University of Helsinki, P.O. Box 63, 00014, Helsinki, Finland.
¹² Department of Surgery, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
¹³ Department of Head and Neck Surgery and Otorhinolaryngology, A.C. Camargo Cancer Center, and University of Sao Paulo Medical School, Department of Head and Neck Surgery, São Paulo, SP, 05402-000, Brazil.
¹⁴ Medical Informatics and Data Analysis Research Group, University of Oulu, Oulu, Finland.
¹⁵ Department of Oral Diagnosis and Graduate Program in Oral Biology, School of Dentistry, University of Campinas, Piracicaba, São Paulo, 13414-018, Brazil.
¹⁶ Faculty of Medicine, Research Program in Systems Oncology, University of Helsinki, Helsinki, Finland.
¹⁷ Department of Otorhinolaryngology - Head and Neck Surgery, University of Helsinki and Helsinki University Hospital, P.O. Box 263, 00029, Helsinki, Finland.
¹⁸ Department of Clinical Sciences, Intervention and Technology, Division of Ear, Nose and Throat Diseases, Karolinska Institutet and Karolinska University Hospital, Stockholm, Sweden.
¹⁹ Institute of Biomedicine, Pathology, University of Turku, 20520, Turku, Finland.
²⁰ Turku University Central Hospital, Turku, Finland.

^# Contributed equally.

Abstract

Background: The clinical significance of tertiary lymphoid structures (TLSs) is not well-documented in early oral tongue squamous cell carcinoma (OTSCC).

Methods: A total of 310 cases of early (cT1-2N0) OTSCC were included in this multicenter study. Assessment of TLSs was conducted on hematoxylin and eosin-stained sections. TLSs were assessed both in the central part of the tumor and at the invasive front area.

Results: The presence of TLSs associated with improved survival of early OTSCC as presented by Kaplan-Meier survival analyses for disease-specific survival (P = 0.01) and overall survival (P = 0.006). In multivariable analyses, which included conventional prognostic factors, the absence of TLSs associated with worse disease-specific survival with a hazard ratio (HR) of 1.96 (95% CI 1.09-3.54; P = 0.025) and poor overall survival (HR 1.66, 95% CI 1.11-2.48; P = 0.014).

Conclusion: Histological evaluation of TLSs predicts survival in early OTSCC. TLSs showed superior prognostic power independent of routine WHO grading and TNM staging system.

Keywords: Early stage; Oral tongue cancer; Survival; Tertiary lymphoid structures.

Publication types

Multicenter Study

MeSH terms

Carcinoma, Squamous Cell* / pathology
Head and Neck Neoplasms*
Humans
Mouth Neoplasms*
Prognosis
Squamous Cell Carcinoma of Head and Neck
Tertiary Lymphoid Structures* / pathology
Tongue Neoplasms* / pathology