Predictors of Local Invasion in Infiltrative Basal Cell Carcinoma: Tumour Budding Outperforms the WHO Subtyping
DOI:
https://doi.org/10.2340/actadv.v104.40172Keywords:
Basal cell carcinoma, Tumor budding, risk assesment, treatment, World Health Organization, classificationAbstract
Tumour budding (TB) correlates with increased local invasion in various neoplasms. Certain basal cell carcinomas (BCCs) exhibit local aggressiveness. Detecting adverse prognostic factors in partial biopsies could aid in identifying cases with heightened local risk. The absolute number of TB (≤ 3 tumour cells) in excision specimens of 271 infiltrative BCCs (0: absent; 1: 1–2 foci; 2: ≥ 3 foci; 3: ≥ 10 foci), the histopathological subtype and depth of infiltration, perineural invasion, and other histological features were evaluated. A significant correlation was found between TB and both depth of infiltration (rho 0.445, p < 0.001) and perineural invasion (p = 0.009). In the multivariate analysis of depth and perineural invasion (multiple regression, stepwise), TB was identified as a significant covariate together with diameter, inflammation, and perineural invasion for the former, and depth for the latter. Conversely, no correlation existed between the WHO histological subtypes (infiltrating, sclerosing, and micronodular), and depth of infiltration or perineural invasion. This study demonstrates the value of TB as a biomarker for local invasiveness in BCC. In routine practice, a count of ≥ 3 TB foci in lesions incompletely excised or with narrow tumour-free surgical margins would be a straightforward and reproducible method to guide BCC treatment.
Downloads
References
Peris K, Fargnoli MC, Garbe C, Kaufmann R, Bastholt L, Seguin NB, et al. Diagnosis and treatment of basal cell carcinoma: European consensus-based interdisciplinary guidelines. Eur J Cancer, 2019; 118: 10-34.
https://doi.org/10.1016/j.ejca.2019.06.003 DOI: https://doi.org/10.1016/j.ejca.2019.06.003
Fernández-Figueras MT, Malvehi J, Tschandl P, Rutten A, Rongioletti F, Requena L, et al. Position paper on a simplified histopathological classification of basal cell carcinoma: results of the European Consensus Project. J Eur Acad Dermatol Venereol 2022; 36: 351-359.
https://doi.org/10.1111/jdv.17849 DOI: https://doi.org/10.1111/jdv.17849
Huang L, Wang X, Pei S, Li X, Dong L, Bian X, et al. Single-cell profiling reveals sustained immune infiltration, surveillance, and tumor heterogeneity in infiltrative basal cell carcinoma. J Invest Dermatol 2023; 143: 2283-2294.
https://doi.org/10.1016/j.jid.2023.04.020 DOI: https://doi.org/10.1016/j.jid.2023.04.020
Pal A, Barrett TF, Paolini R, Parikh A, Puram SV. Partial EMT in head and neck cancer biology: a spectrum instead of a switch. Oncogene 2021; 40: 5049-5065.
https://doi.org/10.1038/s41388-021-01868-5 DOI: https://doi.org/10.1038/s41388-021-01868-5
Zlobec I, Berger MD, Lugli A. Tumour budding and its clinical implications in gastrointestinal cancers. Br J Cancer 2020; 123: 700-708.
https://doi.org/10.1038/s41416-020-0954-z DOI: https://doi.org/10.1038/s41416-020-0954-z
Feakins RM, Loughrey MB, Silver A. Buds, clusters, and transitions in 21st century colorectal carcinoma: revolution or reinvention? J Pathol 2023; 261: 121-124.
https://doi.org/10.1002/path.6173 DOI: https://doi.org/10.1002/path.6173
Imai T. The growth of human carcinoma: a morphological analysis. Fukuoka Igaku Zasshi 1954; 45: 72-102.
Stögbauer F, Beck S, Ourailidis I, Hess J, Poremba C, Lauterbach M, et al. Tumour budding-based grading as independent prognostic biomarker in HPV-positive and HPV-negative head and neck cancer. Br J Cancer 2023; 128: 2295-2306.
https://doi.org/10.1038/s41416-023-02240-y DOI: https://doi.org/10.1038/s41416-023-02240-y
Eckstein M, Matek C, Wagner P, Erber R, Büttner-Herold M, Wild PJ, et al. Proposal for a novel histological scoring system as a potential grading approach for muscle-invasive urothelial bladder cancer correlating with disease aggressiveness and patient outcomes. Eur Urol Oncol 2024; 7: 128-138.
https://doi.org/10.1016/j.euo.2023.07.011 DOI: https://doi.org/10.1016/j.euo.2023.07.011
Ailia MJ, Thakur N, Chong Y, Yim K. Tumor budding in gynecologic cancer as a marker for poor survival: a systematic review and meta-analysis of the perspectives of epithelial-mesenchymal transition. Cancers (Basel) 2022; 14: 1431.
https://doi.org/10.3390/cancers14061431 DOI: https://doi.org/10.3390/cancers14061431
Zombori-Tóth N, Hegedűs F, Almási S, Sejben A, Tiszlavicz L, Furák J, et al. Proposal of a grading system for squamous cell carcinoma of the lung: the prognostic importance of tumour budding, single cell invasion, and nuclear diameter. Virchows Arch 2023; 483: 393-404.
https://doi.org/10.1007/s00428-023-03612-8 DOI: https://doi.org/10.1007/s00428-023-03612-8
Jiang D, Xu S, Zhang C, Hu C, Li L, Zhang M, et al. Association between the expression levels of ADAMTS16 and BMP2 and tumor budding in hepatocellular carcinoma. Oncol Lett 2023; 25: 256.
https://doi.org/10.3892/ol.2023.13842 DOI: https://doi.org/10.3892/ol.2023.13842
Karayannopoulou G, Panteris E, Kanitakis J. Tumour budding is an independent predictive factor of cutaneous squamous-cell carcinoma aggressiveness. Anticancer Res 2020; 40: 2695-2699.
https://doi.org/10.21873/anticanres.14240 DOI: https://doi.org/10.21873/anticanres.14240
Fujimoto M, Yamamoto Y, Takai T, Fujimoto N, Ogawa K, Yoshikawa T, et al. Tumor budding is an objective high-risk factor associated with metastasis and poor clinical prognosis in cutaneous squamous cell carcinoma sized <4 cm. Am J Surg Pathol 2019; 43: 975-983.
https://doi.org/10.1097/PAS.0000000000001284 DOI: https://doi.org/10.1097/PAS.0000000000001284
Gonzalez-Guerrero M, Martínez-Camblor P, Vivanco B, Fernández-Vega I, Munguía-Calzada P, Gonzalez-Gutierrez MP, et al. The adverse prognostic effect of tumor budding on the evolution of cutaneous head and neck squamous cell carcinoma. J Am Acad Dermatol 2017; 76: 1139-1145.
https://doi.org/10.1016/j.jaad.2017.01.015 DOI: https://doi.org/10.1016/j.jaad.2017.01.015
Farah M, Milton DR, Gross ND, Nagarajan P, Gu J, Curry JL, et al. Histopathologic features predictive of metastasis and survival in 230 patients with cutaneous squamous cell carcinoma of the head and neck and non-head and neck locations: a single-center retrospective study. J Eur Acad Dermatol Venereol 2022; 36: 1246-1255.
https://doi.org/10.1111/jdv.18147 DOI: https://doi.org/10.1111/jdv.18147
Lino-Silva LS, Zepeda-Najar C, Caro-Sánchez CH, Herrera-Gómez Á, Salcedo-Hernández RA. Prognostic significance of tumor budding in melanoma. Melanoma Res 2022; 32: 318-323.
https://doi.org/10.1097/CMR.0000000000000839 DOI: https://doi.org/10.1097/CMR.0000000000000839
Zlobec I, Bächli M, Galuppini F, Berger MD, Dawson HE, Nagtegaal ID, et al. Refining the ITBCC tumor budding scoring system with a "zero-budding" category in colorectal cancer. Virchows Arch 2021; 479: 1085-1090
https://doi.org/10.1007/s00428-021-03090-w DOI: https://doi.org/10.1007/s00428-021-03090-w
Messina J, Epstein E, Kossard S, McKenzie C, Patel R, Patterson J, et al. Basal cell carcinoma. In: Elder DE, Massi D, Scolyer RA, Willemze R, editors. WHO classification of skin tumours. Lyon: International Agency for Research on Cancer; 2018: p. 26-34.
Pai RK, Banerjee I, Shivji S, Jain S, Hartman D, Buchanan DD, et al. Quantitative pathologic analysis of digitized images of colorectal carcinoma improves prediction of recurrence-free survival. Gastroenterology 2022; 163: 1531-1546.e8.
https://doi.org/10.1053/j.gastro.2022.08.025 DOI: https://doi.org/10.1053/j.gastro.2022.08.025
Urech M, Kyrgidis A, Argenziano G, Reggiani C, Moscarella E, Longo C, et al. Dermoscopic ulceration is a predictor of basal cell carcinoma response to imiquimod: a retrospective study. Acta Derm Venereol 2017; 97: 117-119.
https://doi.org/10.2340/00015555-2464 DOI: https://doi.org/10.2340/00015555-2464
Published
How to Cite
License
Copyright (c) 2024 Maria Teresa Fernandez-Figueras, Noelia Perez-Muñoz, Luis Puig, Rodolfo Posada-Caez, Rosa Ballester Victoria, Martha Henriquez, Eva Musulen
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
All digitalized ActaDV contents is available freely online. The Society for Publication of Acta Dermato-Venereologica owns the copyright for all material published until volume 88 (2008) and as from volume 89 (2009) the journal has been published fully Open Access, meaning the authors retain copyright to their work.
Unless otherwise specified, all Open Access articles are published under CC-BY-NC licences, allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for non-commercial purposes, provided proper attribution to the original work.