Clinico-pathological correlation of optical fluorescence imaging in oral mucosal lesions.

autofluorescence histomorphometric measurements histopathological correlations optical fluorescence imaging oral mucosal lesions

Journal

Oral diseases
ISSN: 1601-0825
Titre abrégé: Oral Dis
Pays: Denmark
ID NLM: 9508565

Informations de publication

Date de publication:
Sep 2020
Historique:
revised: 22 02 2020
received: 20 10 2019
accepted: 15 03 2020
medline: 22 3 2020
pubmed: 22 3 2020
entrez: 22 3 2020
Statut: ppublish

Résumé

This study aimed to identify clinical and pathological characteristics of oral mucosal lesions that may be predictive of optical autofluorescence imaging patterns. Clinical data and archival histopathological material were collected from patients who presented with at least one oral mucosal lesion and underwent assessment via conventional oral examination, optical autofluorescence imaging and histopathological analysis. An open-source digital pathology image analysis software was used to perform histomorphometric measurements. Classification and regression trees were used to determine histopathological characteristics most predictive of a clinical autofluorescence outcome. Histomorphometric features associated with tissue architecture, epithelial changes, inflammation and vasculature were found to be significantly associated with autofluorescence patterns. Diascopic fluorescence was found to be significantly predicted by lichenoid inflammation and was significantly associated with a diagnosis of oral lichen planus. Loss of autofluorescence with partial blanching was significantly associated with histopathological features noted in dysplastic and malignant lesions. This study provides evidence for the use of diascopic fluorescence as a technique to aid in clinical differentiation of benign inflammatory lesions from potentially malignant pathology. Based on the findings of this study, optical fluorescence imaging is a technique of added value in discernment of oral mucosal lesions, and our results support its clinical use.

Identifiants

pubmed: 32198955
doi: 10.1111/odi.13334
doi:

Types de publication

Journal Article

Langues

eng

Pagination

1230-1239

Informations de copyright

© 2020 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd. All rights reserved.

Références

Amirchaghmaghi, M., Mohtasham, N., Delavarian, Z., Shakeri, M. T., Hatami, M., & Mosannen Mozafari, P. (2018). The diagnostic value of the native fluorescence visualization device for early detection of premalignant/malignant lesions of the oral cavity. Photodiagnosis and Photodynamic Therapy, 21, 19-27. https://doi.org/10.1016/j.pdpdt.2017.10.019
Awan, K., Morgan, P. R., & Warnakulasuriya, S. (2011). Evaluation of an autofluorescence based imaging system (VELscopeTM) in the detection of oral potentially malignant disorders and benign keratoses. Oral Oncology, 47(4), 274-277. https://doi.org/10.1016/j.oraloncology.2011.02.001
Awan, K., & Patil, S. (2015). Efficacy of autofluorescence imaging as an adjunctive technique for examination and detection of oral potentially malignant disorders: A systematic review. The Journal of Contemporary Dental Practice, 16(9), 744-749.
Bankhead, P., Loughrey, M. B., Fernández, J. A., Dombrowski, Y., McArt, D. G., Dunne, P. D., … Hamilton, P. W. (2017). QuPath: Open source software for digital pathology image analysis. Scientific Reports, 7(1), 1-7. https://doi.org/10.1038/s41598-017-17204-5
Betz, C. S., Mehlmann, M., Rick, K., Stepp, H., Grevers, G., Baumgartner, R., & Leunig, A. (1999). Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer. Lasers in Surgery and Medicine, 25(4), 323-334. https://doi.org/10.1002/(SICI)1096-9101(1999)25:4<323:AID-LSM7>3.0.CO;2-P
Betz, C. S., Stepp, H., Janda, P., Arbogast, S., Grevers, G., Baumgartner, R., & Leunig, A. (2002). A comparative study of normal inspection, autofluorescence and 5-ALA-induced PPIX fluorescence for oral cancer diagnosis. International Journal of Cancer, 97(2), 245-252. https://doi.org/10.1002/ijc.1596
Bhatia, N., Matias, M. A. T., & Farah, C. S. (2014). Assessment of a decision making protocol to improve the efficacy of VELscopeTM in general dental practice: A prospective evaluation. Oral Oncology, 50(10), 1012-1019. https://doi.org/10.1016/j.oraloncology.2014.07.002
Bhatia, N., Lalla, Y., Vu, A. N., & Farah, C. S., , (2013). Advances in optical adjunctive aids for visualisation and detection of oral malignant and potentially malignant lesions. Int J Dent, 2013, 194029. https://doi.org/10.1155/2013/194029
Chiang, T. E., Lin, Y. C., Li, Y. H., Wu, C. T., Kuo, C. S., & Chen, Y. W. (2019). Comparative evaluation of autofluorescence imaging and histopathological investigation for oral potentially malignant disorders in Taiwan. Clinical Oral Investigations, 23(5), 2395-2402. https://doi.org/10.1007/s00784-018-2691-8
de Veld, D. C. G., Sterenborg, H. J. C. M., Roodenburg, J. L. N., & Witjes, M. J. H. (2004). Effects of individual characteristics on healthy oral mucosa autofluorescence spectra. Oral Oncology, 40(8), 815-823. https://doi.org/10.1016/j.oraloncology.2004.02.006
El-Naggar, A. K., Chan, J. K. C., Takata, T., Grandis, J. R., & Slootweg, P. J. (2017). The fourth edition of the head and neck World Health Organization blue book: Editors’ perspectives. Human Pathology, 66, 10-12. https://doi.org/10.1016/j.humpath.2017.05.014
Farah, C. S., & Fox, S. A. (2019). Dysplastic oral leukoplakia is molecularly distinct from leukoplakia without dysplasia. Oral Diseases, 25(7), 1715-1723. https://doi.org/10.1111/odi.13156
Farah, C. S., Kordbacheh, F., John, K., Bennett, N., & Fox, S. A. (2017). Molecular classification of autofluorescence excision margins in oral potentially malignant disorders. Oral Diseases, 24(5), 732-740. https://doi.org/10.1111/odi.12818
Farah, C. S., McIntosh, L., Georgiou, A., & McCullough, M. J. (2012). Efficacy of tissue autofluorescence imaging (VELScope) in the visualization of oral mucosal lesions. Head & Neck, 34(6), 856-862. https://doi.org/10.1002/hed.21834
Farah, C. S., Woo, S., Zain, R. B., Sklavounou, A., McCullough, M. J., & Lingen, M. (2014). Oral cancer and oral potentially malignant disorders. International Journal of Dentistry, 2014, 6. https://doi.org/10.1155/2014/853479
Fujii, S., Yamazaki, M., Muto, M., & Ochiai, A. (2010). Microvascular irregularities are associated with composition of squamous epithelial lesions and correlate with subepithelial invasion of superficial-type pharyngeal squamous cell carcinoma. Histopathology, 56(4), 510-522. https://doi.org/10.1111/j.1365-2559.2010.03512.x
Gaykalova, D. A., Mambo, E., Choudhary, A., Houghton, J., Buddavarapu, K., Sanford, T., … Sun, W. (2014). Novel insight into mutational landscape of head and neck squamous cell carcinoma. PLoS ONE, 9(3), e93102. https://doi.org/10.1371/journal.pone.0093102
Jayaprakash, V., Sullivan, M., Merzianu, M., Rigual, N. R., Loree, T. R., Popat, S. R., … Reid, M. E. (2009). Autofluorescence-guided surveillance for oral cancer. Cancer Prevention Research, 2(11), 966-974. https://doi.org/10.1158/1940-6207.CAPR-09-0062
Kordbacheh, F., Bhatia, N., & Farah, C. S. (2016). Patterns of differentially expressed genes in oral mucosal lesions visualised under autofluorescence (VELscope(TM)). Oral Diseases, 22(4), 285-296. https://doi.org/10.1111/odi.12438
Kujan, O., Oliver, R. J., Khattab, A., Roberts, S. A., Thakker, N., & Sloan, P. (2006). Evaluation of a new binary system of grading oral epithelial dysplasia for prediction of malignant transformation. Oral Oncology, 42(10), 987-993. https://doi.org/10.1016/j.oraloncology.2005.12.014
Lalla, Y., Matias, M. A. T., & Farah, C. S. (2015). Oral mucosal disease in an Australian urban Indigenous community using autofluorescence imaging and reflectance spectroscopy. Australian Dental Journal, 60(2), 216-224. https://doi.org/10.1111/adj.12320
Lalla, Y., Matias, M. A. T., & Farah, C. S. (2016). Assessment of oral mucosal lesions with autofluorescence imaging and reflectance spectroscopy. The Journal of the American Dental Association, 147(8), 650-660. https://doi.org/10.1016/j.adaj.2016.03.013
Lane, P. M., Gilhuly, T., Whitehead, P., Zeng, H., Poh, C. F., Ng, S., … MacAulay, C. E. (2006). Simple device for the direct visualization of oral-cavity tissue fluorescence. Journal of Biomedical Optics, 11(2), 024006. https://doi.org/10.1117/1.2193157
Lin, H.-C., Lee, H.-S., Chiueh, T.-S., Lin, Y.-C., Lin, H.-A., Lin, Y.-C., … Meng, E. N. (2015). Histopathological assessment of inflammation and expression of inflammatory markers in patients with ketamine-induced cystitis. Molecular Medicine Reports, 11(4), 2421-2428. https://doi.org/10.3892/mmr.2014.3110
Marzouki, H. Z., Tuong Vi Vu, T., Ywakim, R., Chauvin, P., Hanley, J., & Kost, K. M. (2012). Use of fluorescent light in detecting malignant and premalignant lesions in the oral cavity: A prospective, single-blind study. Journal of Otolaryngology - Head & Neck Surgery, 41(3), 164-168.
Mehrotra, R., Singh, M., Thomas, S., Nair, P., Pandya, S., Nigam, N. S., & Shukla, P. (2010). A Cross-sectional study evaluating chemiluminescence and autofluorescence in the detection of clinically innocuous precancerous and cancerous oral lesions. The Journal of the American Dental Association, 141(2), 151-156. https://doi.org/10.14219/jada.archive.2010.0132
Min, W., Lu, S., Chong, S., Roy, R., Holtom, G. R., & Xie, X. S. (2009). Imaging chromophores with undetectable fluorescence by stimulated emission microscopy. Nature, 461(7267), 1105-1109. https://doi.org/10.1038/nature08438
Pavlova, I., Williams, M., El-Naggar, A., Richards-Kortum, R., & Gillenwater, A. (2008). Understanding the biological basis of autofluorescence imaging for oral cancer detection: High-resolution fluorescence microscopy in viable tissue. Clinical Cancer Research, 14(8), 2396-2404. https://doi.org/10.1158/1078-0432.CCR-07-1609
Pazouki, S., Chisholm, D. M., Adi, M. M., Carmichael, G., Farquharson, M., Ogden, G. R., & Schor, A. M. (1997). The association between tumour progression and vascularity in the oral mucosa. The Journal of Pathology, 183(1), 39-43. https://doi.org/10.1002/(SICI)1096-9896(199709)183:1<39:AID-PATH1088>3.0.CO;2-L
Pérez-López, D., Pena-Cristóbal, M., Otero-Rey, E.-M., Tomás, I., & Blanco-Carrión, A. (2016). Clinical value of diascopy and other non-invasive techniques on differential diagnosis algorithms of oral pigmentations: A systematic review. Journal of Clinical and Experimental Dentistry, 8(4), e448-e458. https://doi.org/10.4317/jced.53005
Petruzzi, M., Lucchese, A., Nardi, G. M., Lauritano, D., Favia, G., Serpico, R., & Grassi, F. R. (2014). Evaluation of autofluorescence and toluidine blue in the differentiation of oral dysplastic and neoplastic lesions from non dysplastic and neoplastic lesions: A cross-sectional study. Journal of Biomedical Optics, 19(7), 076003. https://doi.org/10.1117/1.JBO.19.7.076003
Poh, C. F., Anderson, D. W., Durham, J. S., Chen, J., Berean, K. W., MacAulay, C. E., & Rosin, M. P. (2016). Fluorescence visualization-guided surgery for early-stage oral cancer. JAMA Otolaryngology-Head & Neck Surgery, 142(3), 209-216. https://doi.org/10.1001/jamaoto.2015.3211
Poh, C. F., Zhang, L., Anderson, D. W., Durham, J. S., Williams, P. M., Priddy, R. W., … Rosin, M. P. (2006). Fluorescence visualization detection of field alterations in tumor margins of oral cancer patients. Clinical Cancer Research, 12(22), 6716-6722. https://doi.org/10.1158/1078-0432.CCR-06-1317
R Core Team (2014). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/.
Raica, M., Cimpean, A. M., & Ribatti, D. (2009). Angiogenesis in pre-malignant conditions. European Journal of Cancer, 45(11), 1924-1934. https://doi.org/10.1016/j.ejca.2009.04.007
Rana, M., Zapf, A., Kuehle, M., Gellrich, N.-C., & Eckardt, A. M. (2012). Clinical evaluation of an autofluorescence diagnostic device for oral cancer detection: A prospective randomized diagnostic study. European Journal of Cancer Prevention, 21(5), 460-466. https://doi.org/10.1097/CEJ.0b013e32834fdb6d
Rethman, M. P., Carpenter, W., Cohen, E. E. W., Epstein, J., Evans, C. A., Flaitz, C. M., … Meyer, D. M. (2010). Evidence-based clinical recommendations regarding screening for oral squamous cell carcinomas. The Journal of the American Dental Association, 141(5), 509-520. https://doi.org/10.14219/jada.archive.2010.0223
Sawan, D., & Mashlah, A. (2015). Evaluation of premalignant and malignant lesions by fluorescent light (VELscope). Journal of International Society of Preventive & Community Dentistry, 5(3), 248-324.
Scheer, M., Fuss, J., Derman, M. A., Kreppel, M., Neugebauer, J., Rothamel, D., … Zoeller, J. E. (2016). Autofluorescence imaging in recurrent oral squamous cell carcinoma. Oral & Maxillofacial Surgery, 20(1), 27-33. https://doi.org/10.1007/s10006-015-0520-7
Tiwari, L., Kujan, O., & Farah, C. S. (2019). Optical fluorescence imaging in oral cancer and potentially malignant disorders: A systematic review. Oral Diseases, 00, 1-20. https://doi.org/10.1111/odi.13071
von Elm, E., Altman, D. G., Egger, M., Pocock, S. J., Gøtzsche, P. C., Vandenbroucke, J. P., & Initiative, S. T. R. O. B. E. (2008). The strengthening the reporting of observational studies in epidemiology (STROBE) statement: Guidelines for reporting observational studies. Journal of Clinical Epidemiology, 61(4), 344-349. https://doi.org/10.1016/j.jclinepi.2007.11.008
Westra, W. H., & Sidransky, D. (2006). Fluorescence visualization in oral neoplasia: Shedding light on an old Problem. Clinical Cancer Research, 12(22), 6594-6597. https://doi.org/10.1158/1078-0432.CCR-06-2253
Wu, X., & Kumar, V. (2009). The top ten algorithms in data mining. Boca Raton, FL: CRC Press.

Auteurs

Lalima Tiwari (L)

UWA Dental School, University of Western Australia, Nedlands, WA, Australia.

Omar Kujan (O)

UWA Dental School, University of Western Australia, Nedlands, WA, Australia.

Camile S Farah (CS)

Australian Centre for Oral Oncology Research & Education, Nedlands, WA, Australia.
Oral, Maxillofacial and Dental Surgery, Fiona Stanley Hospital, Murdoch, WA, Australia.

Classifications MeSH