Worst Pattern of Perineural Invasion Redefines the Spatial Localization of Nerves in Oral Squamous Cell Carcinoma

As a key histopathological characteristic of tumor invasion, perineural invasion (PNI) assists tumor dissemination, whereas the current definition of PNI by dichotomy is not accurate and the prognostic value of PNI has not reached consensus. To define PNI status in each patient when mixed types of P...

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Autores principales:	Yong Fu, Xinwen Zhang, Zhuang Ding, Nisha Zhu, Yuxian Song, Xiaoxin Zhang, Yue Jing, Yijun Yu, Xiaofeng Huang, Lei Zhang, Qingang Hu, Yanhong Ni, Liang Ding
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	tumor-nerve interaction worst pattern of perineural invasion (WPNI) oral squamous cell carcinoma (OSCC) prognostic biomarker immune balance Neoplasms. Tumors. Oncology. Including cancer and carcinogens RC254-282
Acceso en línea:	https://doaj.org/article/fe6e040b798441b58899f00dc0e848eb
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spelling	oai:doaj.org-article:fe6e040b798441b58899f00dc0e848eb2021-12-01T13:26:09ZWorst Pattern of Perineural Invasion Redefines the Spatial Localization of Nerves in Oral Squamous Cell Carcinoma2234-943X10.3389/fonc.2021.766902https://doaj.org/article/fe6e040b798441b58899f00dc0e848eb2021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fonc.2021.766902/fullhttps://doaj.org/toc/2234-943XAs a key histopathological characteristic of tumor invasion, perineural invasion (PNI) assists tumor dissemination, whereas the current definition of PNI by dichotomy is not accurate and the prognostic value of PNI has not reached consensus. To define PNI status in each patient when mixed types of PNI occurred simultaneously, we here further subclassified the traditional PNI in 183 patients with oral squamous cell carcinoma (OSCC). The spatial localization of nerves in OSCC microenvironment was thoroughly evaluated and successfully concluded into four types of PNI: 0, tumor cells away from nerves; 1, tumor cells encircling nerves less than 33%; 2, tumor cells encircling nerves at least 33%; and 3, tumor cells infiltrating into nerve sheathes. Sequentially, patients were stratified by single and mixed types of PNI. Traditionally, types 0 and 1 were defined as PNI−, while types 2 and 3 were PNI+, which predicted shorter survival time. When multiple types of PNI existed within one tumor, patients with higher score of PNI types tended to have a relatively worse prognosis. Therefore, to define the status of PNI more precisely, the new variable worst pattern of PNI (WPNI) was proposed, which was taken as the highest score of PNI types present in each patient no matter how focal. Results showed that patients with WPNI 1 had longest survival time, and WPNI 2 correlated with better overall survival (p = 0.02), local-regional recurrence-free survival (p = 0.03), and distant metastasis-free survival (p = 0.046) than WPNI 3. Multivariate Cox analysis confirmed that only WPNI 3 could independently predict patients’ prognosis, which could be explained by a more damaged immune response in WPNI 3 patients with less CD3+CD8+ T cells and CD19+ B cells. Conclusively, WPNI by trichotomy provide more meticulous and precise pathological information for tumor-nerve interactions in OSCC patients.Yong FuXinwen ZhangZhuang DingNisha ZhuYuxian SongXiaoxin ZhangYue JingYijun YuXiaofeng HuangLei ZhangQingang HuYanhong NiLiang DingFrontiers Media S.A.articletumor-nerve interactionworst pattern of perineural invasion (WPNI)oral squamous cell carcinoma (OSCC)prognostic biomarkerimmune balanceNeoplasms. Tumors. Oncology. Including cancer and carcinogensRC254-282ENFrontiers in Oncology, Vol 11 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	tumor-nerve interaction worst pattern of perineural invasion (WPNI) oral squamous cell carcinoma (OSCC) prognostic biomarker immune balance Neoplasms. Tumors. Oncology. Including cancer and carcinogens RC254-282
spellingShingle	tumor-nerve interaction worst pattern of perineural invasion (WPNI) oral squamous cell carcinoma (OSCC) prognostic biomarker immune balance Neoplasms. Tumors. Oncology. Including cancer and carcinogens RC254-282 Yong Fu Xinwen Zhang Zhuang Ding Nisha Zhu Yuxian Song Xiaoxin Zhang Yue Jing Yijun Yu Xiaofeng Huang Lei Zhang Qingang Hu Yanhong Ni Liang Ding Worst Pattern of Perineural Invasion Redefines the Spatial Localization of Nerves in Oral Squamous Cell Carcinoma
description	As a key histopathological characteristic of tumor invasion, perineural invasion (PNI) assists tumor dissemination, whereas the current definition of PNI by dichotomy is not accurate and the prognostic value of PNI has not reached consensus. To define PNI status in each patient when mixed types of PNI occurred simultaneously, we here further subclassified the traditional PNI in 183 patients with oral squamous cell carcinoma (OSCC). The spatial localization of nerves in OSCC microenvironment was thoroughly evaluated and successfully concluded into four types of PNI: 0, tumor cells away from nerves; 1, tumor cells encircling nerves less than 33%; 2, tumor cells encircling nerves at least 33%; and 3, tumor cells infiltrating into nerve sheathes. Sequentially, patients were stratified by single and mixed types of PNI. Traditionally, types 0 and 1 were defined as PNI−, while types 2 and 3 were PNI+, which predicted shorter survival time. When multiple types of PNI existed within one tumor, patients with higher score of PNI types tended to have a relatively worse prognosis. Therefore, to define the status of PNI more precisely, the new variable worst pattern of PNI (WPNI) was proposed, which was taken as the highest score of PNI types present in each patient no matter how focal. Results showed that patients with WPNI 1 had longest survival time, and WPNI 2 correlated with better overall survival (p = 0.02), local-regional recurrence-free survival (p = 0.03), and distant metastasis-free survival (p = 0.046) than WPNI 3. Multivariate Cox analysis confirmed that only WPNI 3 could independently predict patients’ prognosis, which could be explained by a more damaged immune response in WPNI 3 patients with less CD3+CD8+ T cells and CD19+ B cells. Conclusively, WPNI by trichotomy provide more meticulous and precise pathological information for tumor-nerve interactions in OSCC patients.
format	article
author	Yong Fu Xinwen Zhang Zhuang Ding Nisha Zhu Yuxian Song Xiaoxin Zhang Yue Jing Yijun Yu Xiaofeng Huang Lei Zhang Qingang Hu Yanhong Ni Liang Ding
author_facet	Yong Fu Xinwen Zhang Zhuang Ding Nisha Zhu Yuxian Song Xiaoxin Zhang Yue Jing Yijun Yu Xiaofeng Huang Lei Zhang Qingang Hu Yanhong Ni Liang Ding
author_sort	Yong Fu
title	Worst Pattern of Perineural Invasion Redefines the Spatial Localization of Nerves in Oral Squamous Cell Carcinoma
title_short	Worst Pattern of Perineural Invasion Redefines the Spatial Localization of Nerves in Oral Squamous Cell Carcinoma
title_full	Worst Pattern of Perineural Invasion Redefines the Spatial Localization of Nerves in Oral Squamous Cell Carcinoma
title_fullStr	Worst Pattern of Perineural Invasion Redefines the Spatial Localization of Nerves in Oral Squamous Cell Carcinoma
title_full_unstemmed	Worst Pattern of Perineural Invasion Redefines the Spatial Localization of Nerves in Oral Squamous Cell Carcinoma
title_sort	worst pattern of perineural invasion redefines the spatial localization of nerves in oral squamous cell carcinoma
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/fe6e040b798441b58899f00dc0e848eb
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Worst Pattern of Perineural Invasion Redefines the Spatial Localization of Nerves in Oral Squamous Cell Carcinoma

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