2024_07_05_470c731599753ceca218g

Prognostic implications of mucosal and deep margin distances according to -status in oral tongue squamous cell carcinoma: A single-center retrospective study
根据口腔舌鳞状细胞癌状态的粘膜和深缘距离的预后影响：一项单中心回顾性研究

Department of Surgery, University Cancer Institute of Toulouse - Oncopole, Toulouse, France

图卢兹大学癌症研究所外科系 - Oncopole，图卢兹，法国

Department of Ear, Nose & Throat Surgery, Toulouse University Hospital - Larrey Hospital, Toulouse, France

图卢兹大学医院耳鼻喉外科 - 法国图卢兹拉里医院

Department of Biostatistics, Claudius Regaud Institute, University Cancer Institute of Toulouse - Oncopole, Toulouse, France

图卢兹大学癌症研究所克劳迪乌斯·雷戈研究所生物统计学系 - 法国图卢兹市Oncopole

Department of Maxillofacial Surgery, Toulouse University Hospital - Pierre Paul Riquet Hospital, Toulouse, France

图卢兹大学医院颌面外科 - 法国图卢兹皮埃尔·保罗·里凯医院

Department of Pathology, University Cancer Institute Oncopole and Toulouse University Hospital, Toulouse, France

法国图卢兹肿瘤大学癌症研究所和图卢兹大学医院病理学系

Correspondence 通信

Emilien Chabrillac, Department of Surgery, University Cancer Institute of Toulouse - Oncopole, 1 avenue Irène Joliot-Curie, 31100 Toulouse, France. Email: chabrillac.emilien@iuctoncopole.fr
Emilien Chabrillac，图卢兹大学癌症研究所外科 - Oncopole，1 avenue Irène Joliot-Curie，31100 Toulouse，France。电子邮件： chabrillac.emilien@iuctoncopole.fr

Section Editor: Benjamin Judson
栏目编辑：本杰明·贾德森

Abstract 抽象

Objective: To elucidate the prognostic implications of mucosal and deep margin distances in oral tongue squamous cell carcinoma (OTSCC), and to assess a different margin cut-off value in T1-T2 versus T3-T4 tumors.
目的：探讨口腔舌鳞状细胞癌（OTSCC）黏膜和深缘距离的预后意义，并评估T1-T2与T3-T4肿瘤的不同切缘临界值。

Methods: This single-center retrospective study included 223 patients who received surgery for a primary OTSCC between January 2017 and December 2021.
方法：这项单中心回顾性研究纳入了 2017 年 1 月至 2021 年 12 月期间接受原发性 OTSCC 手术的 223 例患者。

Results: Multivariable analysis showed that deep margin distance in T1-T2 tumors and in T3-T4 tumors was significantly associated with better RFS and OS. Mucosal and deep margin distances were globally clinically useful for 2-year RFS prediction of T1-T2 tumors, for which deep margins seemed to have more clinical utility than mucosal margins. The influence of margin distances on 2-year RFS seemed greater for T1-T2 tumors than T3-T4 tumors.
结果：多变量分析显示，T1-T2 肿瘤和 T3-T4 肿瘤的深切缘距离与较好的 RFS 和 OS 显著相关。黏膜和深切缘距离对 T1-T2 肿瘤的 2 年 RFS 预测具有全球临床意义，深切缘似乎比黏膜边缘更具临床效用。对于 T1-T2 肿瘤，边缘距离对 2 年 RFS 的影响似乎大于 T3-T4 肿瘤。

Conclusion: Mucosal and deep margin distances were associated with OS and RFS in OTSCC. Shorter deep margin distances may be aimed for in T1-T2 versus T3-T4 tumors.
结论：OTSCC黏膜和深缘距离与OS和RFS相关。与 T3-T4 肿瘤相比，T1-T2 的深切缘距离可能更短。

KEYWORDS 关键字

glossectomy, margin, recurrence, squamous cell carcinoma, tongue cancer
舌切除术、边缘、复发、鳞状细胞癌、舌癌

1 | INTRODUCTION 1 |介绍

Head and neck cancers are the sixth cancer worldwide,

and among them oral cavity squamous cell carcinoma (SCC) is by far the most common cancer of head and neck, accounting for

of all new cancers.

The mainstay of their treatment is primary surgery. When excision margins are "close" or involved, current recommendation suggests re-resection or adjuvant treatment with radiotherapy (RT) or chemoradiotherapy (CRT).

Surgical margins is one of the main prognostic factors for local control and survival in oral cavity cancers,

and more specifically in tongue SCC.

However, many other prognostic factors are involved, and the decision for adjuvant treatment relies on several factors, for example,

-status, tumor differentiation, perineural invasion (PNI), and lymphovascular emboli (LVE).

头颈癌是全球第六大癌症，

其中口腔鳞状细胞癌（SCC）是迄今为止最常见的头颈癌，

占所有新发癌症的比重。

他们的主要治疗是初次手术。当切缘“接近”或受累时，目前的建议建议重新切除或用放疗（RT）或放化疗（CRT）辅助治疗。

手术切缘是口腔癌局部控制和生存的主要预后因素之一，

更具体地说是舌鳞状细胞癌。

然而，还涉及许多其他预后因素，辅助治疗的决定取决于几个因素，例如

状态、肿瘤分化、神经周围浸润（PNI）和淋巴血管栓塞（LVE）。

While all oral cavity subsites are pooled in the 8th edition of the TNM staging system of the American Joint Committee on Cancer (AJCC), it is proven that all prognostic factors do not carry the same importance and incidence among oral cavity subsites.

In the era of precision medicine, some of these subsites should be studied separately.
虽然所有口腔亚位点都汇总在美国癌症联合委员会（AJCC）第 8 版 TNM 分期系统中，但事实证明，所有预后因素在口腔亚位点中的重要性和发生率并不相同。

在精准医学时代，其中一些亚位点应该单独研究。

Practices vary among centers regarding macroscopic and microscopic surgical margin distances.

Since it is difficult to find the best balance between oncological safety and morbidity of the surgery, the optimal surgical margin threshold in oral cavity SCC is still debated. The most recent meta-analysis tends to favor a

threshold, however without distinguishing mucosal and deep margins, and regardless of tumor-related factors, for example, T-status, PNI, worst pattern of invasion.

关于宏观和微观手术切缘距离的实践因中心而异。

由于很难在肿瘤学安全性和手术发病率之间找到最佳平衡，因此口腔鳞状细胞癌的最佳手术切缘阈值仍存在争议。最近的荟萃分析倾向于设定

阈值，但不区分黏膜和深缘，也不考虑肿瘤相关因素，例如 T 状态、PNI、最差的浸润模式。

With regards to oral tongue SCC, a

threshold has historically been considered as a "negative" margin and known to yield satisfactory oncologic outcomes, however with few studies differentiating T1-T2 and T3-T4 tumors.

More recently, literature showed a trend toward suggesting narrower margin thresholds, up to

regardless of T-status.

large multicentric study by Otsuru et al. with robust methods analyzed receiver operating characteristic curves and suggested a

mucosal margin threshold and a

deep margin threshold for better local control in T1-T2 oral tongue SCC.

Thus, we proposed a clinically applicable threshold inspired by the

threshold from the literature review by Spence et al.

and by rounding up the 3.1and

thresholds of the Otsuru study, that is,

for both mucosal and deep margins in T1-T2 tumors, and

for both mucosal and deep margins in T3-T4 tumors.
关于口腔舌鳞状细胞癌，

阈值历来被认为是“阴性”边缘，并且已知会产生令人满意的肿瘤学结果，但很少有研究区分 T1-T2 和 T3-T4 肿瘤。

2 | MATERIALS AND METHODS
2 |材料与方法

This single-center retrospective study was conducted in a comprehensive cancer center. Included patients received primary surgical treatment for a SCC arising from the oral tongue between January 2017 and December 2021. The study started 2 years after the last included patient was treated in order to theoretically have a minimum of 2 years of follow-up. Patients were operated in two different departments, however all pathological analyses were carried out in the same pathology department. Exclusion criteria were as follows: recurrent tumor, history of neck irradiation, history of another head and neck cancer in the past 5 years, distant metastasis at diagnosis. Specimens with fragmented tumor resection and/or multiple margins harvested (

margins or shorter dimension

) were also excluded as it may decrease the reliability of margins analysis given the complex threedimensional anatomy.

这项单中心回顾性研究是在综合癌症中心进行的。纳入的患者在 2017 年 1 月至 2021 年 12 月期间接受了口腔舌鳞状细胞癌的初级手术治疗。该研究在最后一名纳入的患者接受治疗 2 年后开始，理论上至少进行 2 年的随访。患者在两个不同的科室进行手术，但所有病理分析均在同一病理科室进行。排除标准如下：复发性肿瘤、颈部照射史、过去 5 年内另一种头颈癌病史、诊断时远处转移。具有碎片肿瘤切除和/或收获多个边缘（

边缘或更短尺寸

）的标本也被排除在外，因为考虑到复杂的三维解剖结构，这可能会降低边缘分析的可靠性。

Data were collected in the patients' electronic medical record by a senior investigator (VP). They included demographics, comorbidities, smoking status, alcohol abuse, cancer characteristics (location, local extension), treatment data (type of surgery, reconstruction, adjuvant treatment), pathological data (TNM staging according to AJCC 8th edition, superficial and deep excisional margins, pathological prognostic factors), and follow-up data (recurrence and survival).
数据由高级研究员（VP）在患者的电子病历中收集。它们包括人口统计学、合并症、吸烟状况、酗酒、癌症特征（位置、局部扩展）、治疗数据（手术类型、重建、辅助治疗）、病理数据（根据 AJCC 第 8 版的 TNM 分期、浅切缘和深切缘、病理预后因素）和随访数据（复发和生存）。

The primary treatment of resectable tongue SCC was the same in both departments, that is, wide local excision with

of macroscopic superficial margins. Intraoperative margins for frozen section analysis were not routinely harvested at either site. In cases where the intraoperative examination of the specimen (ex vivo) by the surgeon showed insufficient margins, additional margins were harvested. In cases of close or involved resection margins on permanent section analysis, the decision to perform further resection was made on a case-by-case basis as recommended by the multidisciplinary meeting. Adjuvant RT or CRT was offered to T3 and

patients as well as

patients with adverse pathological features (close or positive margins, PNI, LVE), in accordance with international guidelines.

两个科室对可切除舌鳞状细胞癌的主要治疗相同，即大范围局部切除，

肉眼下浅缘。冷冻切片分析的术中切缘在任一部位均未常规采集。如果外科医生对标本的术中检查（离体）显示余量不足，则收获额外的余量。在永久性切片分析中切除边缘接近或受累的情况下，根据多学科会议的建议，根据具体情况决定进行进一步切除。根据国际指南，向 T3 和

患者以及

/或

具有不良病理特征（切缘接近或阳性、PNI、LVE）的患者提供辅助 RT 或 CRT。

Specimen were fixed in formalin, dehydrated with an alcohol gradient, and embedded in paraffin. Fivemicrometer-thick sections were obtained with a microtome, stained with hematoxylin-eosin, and viewed under an optical microscope (Leica DM3000, Leica Microsystems, Inc., Wetzlar, Germany). Pathologists measured the resection margins in five directions (anterior, posterior, lateral, medial, deep), except in cases in which reliable measurement was impossible, for example, the anterior/ lateral margin in mandibulectomy specimens. Margins distances were calculated from the invasive component of the tumor. Only the presence of invasive SCC classified margins as "positive," as opposed to dysplasia and carcinoma in situ.
将标本固定在福尔马林中，用醇梯度脱水，并包埋在石蜡中。用切片机获得五微米厚的切片，用苏木精-伊红染色，并在光学显微镜下观察（Leica DM3000，Leica Microsystems，Inc.，Wetzlar，Germany）。病理学家在五个方向（前、后、外侧、内侧、深部）测量切除边缘，除非无法可靠测量，例如下颌切除术标本中的前/外侧边缘。从肿瘤的侵袭性成分计算边缘距离。只有浸润性鳞状细胞癌的存在将边缘归类为“阳性”，而不是异型增生和原位癌。

In accordance with the existing literature,

a clinically applicable margin threshold was chosen for assessment of clinical relevance, that is,

for both mucosal and deep margins in T1-T2 tumors and

for both mucosal and deep margins in T3-T4 tumors.
根据现有文献，

选择临床适用的边缘阈值来评估临床相关性，即

T1-T2 肿瘤的粘膜和深缘以及

T3-T4 肿瘤的粘膜和深缘。

This study was conducted within a General Data Protection Regulation-compliant and secure system, in accordance with the French legal framework of MR-004 set up by the National Commission on Informatics and Liberty. This study was recorded in the Health Data Hub and received approval by the local research committee (reference: F20230315180652).
本研究是在符合《通用数据保护条例》的安全系统中进行的，该系统符合国家信息学和自由委员会建立的法国 MR-004 法律框架。这项研究被记录在健康数据中心，并获得了当地研究委员会的批准（参考：F20230315180652）。

2.1 | Statistical analysis
2.1 |统计分析

Continuous variables were summarized using median and range (min-max) and categorical variable with number and percentages. Missing data were described for all variables. Recurrence-free survival (RFS) was defined as the time between the date of surgery and the date of first recurrence or death. Patients still alive and without recurrence were censored at the date of last contact. Overall survival (OS) was defined as the time between the date of surgery and the date of death or censored at the date of last contact. Disease-specific survival (DSS) was defined as the time between the date of surgery and the date of cancer-related death. Patients still alive were censored at the date of last contact and patients who died of other causes were censored at their date of death. Local-recurrence-free survival was defined as the time between the date of surgery and the date of local recurrence. Patients still alive and without local recurrence were censored at their date of last contact, and those who had any other event (death or other type of recurrence) were censored at the date of occurrence of this other event. All survival rates were estimated by the Kaplan-Meier method with their

confidence interval (

CI). Univariable and multivariable analyses were performed using the Logrank test and Cox proportional hazards model, respectively. Variable selection for multivariable analysis was based on clinical relevance and results of univariable analyses.
使用中位数和范围（最小值-最大值）和带有数量和百分比的分类变量对连续变量进行汇总。描述了所有变量的缺失数据。无复发生存期（RFS）定义为手术日期与首次复发或死亡日期之间的时间。仍然活着且没有复发的患者在最后一次接触之日被审查。总生存期（OS）定义为手术日期和死亡日期之间的时间，或在最后一次接触之日进行删失。疾病特异性生存期（DSS）定义为手术日期和癌症相关死亡日期之间的时间。仍然活着的患者在最后一次接触之日被审查，死于其他原因的患者在死亡之日被审查。局部无复发生存期定义为手术日期和局部复发日期之间的时间。仍然活着且没有局部复发的患者在最后一次接触之日被审查，而那些有任何其他事件（死亡或其他类型的复发）的患者在发生其他事件之日被审查。所有存活率均采用Kaplan-Meier方法及其

置信区

间（CI）估计。单变量和多变量分析分别使用 Logrank 检验和 Cox 比例风险模型进行。多变量分析的变量选择基于临床相关性和单变量分析的结果。

The clinical usefulness of margins (mucosal and deep) was assessed using decision curve analysis (DCA). This method calculates the net benefit for both margins on the RFS at 1 and 2 years and displays it graphically to compare to scenes where all patients recurred/died or none at 1 and 2 years.
使用决策曲线分析（DCA）评估边缘（粘膜和深部）的临床有用性。该方法计算 1 年和 2 年时 RFS 两个边缘的净收益，并以图形方式显示，以与所有患者在 1 年和 2 年复发/死亡或无复发/死亡的场景进行比较。

Statistical tests were two-sided and

-value

was considered significant. All statistical analyses were carried out using STATA version 18 software.
统计检验是双面的，

-值

被认为是显著的。所有统计分析均使用STATA第18版软件进行。

3 | RESULTS 3 |结果

A total of 223 patients were included. Most of them were males

, sex ratio

), with a median age at surgery of 62 years (21-94). They were active or former smokers in

and

of cases, respectively. Tobacco exposure exceeded 20 pack-years among

of the active or former smokers. The prevalence of past and active alcohol abuse was

and

, respectively.
共纳入223例患者。他们中的大多数是男性

，性别比例

），手术时的中位年龄为62岁（21-94岁）。他们分别是活跃或曾经的吸烟者

。活跃或既往吸烟者的烟草暴露时间超过20包年

。既往酗酒和现役酗酒的患病率分别为

和

。

Oral tongue SCC were unilateral in

of cases and bilateral in the remaining

. Tumors involved the floor of the mouth, base of tongue, gingiva, tonsillar region/ pillars, and buccal mucosa in

, and

. A mandibulectomy was performed in

of patients. A pull-through approach was required in

of cases. Defect coverage was achieved with primary closure, pedicled or free flap in

, and

of cases, respectively. The neck treatment was as follows: bilateral neck dissection (

), unilateral neck dissection

), sentinel lymph node biopsy (

), or none

). Adjuvant treatment was carried out in

of patients and consisted of RT alone (

) or CRT (

). When performed, RT was delivered to the tumor bed in all cases, and to the neck in

of patients.
口腔舌鳞状细胞癌在病例中

为单侧，其余

病例为双侧。肿瘤累及口腔底部、舌根、牙龈、扁桃体区域/支柱和颊粘膜。

对患者进行了下颌骨切除术。

在一些情况下，需要采取直通式方法。缺损覆盖率分别通过一期闭合、带蒂或游离皮瓣实现

。颈部治疗如下：双侧颈部清扫术（

）、单侧颈部清扫

术、前哨淋巴结活检（

）、或无

）。对

患者进行辅助治疗，包括单独放疗（

）或 CRT （

）。进行放疗时，在所有病例中，放疗都被输送到肿瘤床，并被输送到患者的颈部

。

Pathological outcomes are displayed in Table 1. When taking into account re-resections harvested intraoperatively, mucosal and deep margins were positive in

and

of definitive pathological examinations, respectively. Margin distances on histology are shown in Table 2.
病理结果见表1。当考虑到术中收获的重新切除时，粘膜和深缘分别在

确定性病理检查中呈

阳性。组织学的切缘距离如表2所示。

After a median follow-up of 37.5 months (

[34.3-42.8]),

of patients had presented with a recurrence. The initial recurrence was local, regional, and/or distant metastasis in

, and

of cases, respectively. Among the

of patients who died during the study period,

of deaths were related to the disease. The 5 -year OS and RFS were

(

[63.7-79.1]) and

(95%CI [52.8-68.5]), respectively. The 3 -year DSS and LRFS were

(

CI [79.490.0]) and

(

CI [82.1-92.0]), respectively. Kaplan-Meier estimates of RFS according to surgical margin distance and T-status are shown in Figure 1.
中位随访37.5个月（

[34.3-42.8]）后，

患者出现复发。最初的复发分别是

局部、区域和/或远处转移。

在研究期间死亡的患者中，

死亡与疾病有关。5年OS和RFS分别为

（

63.7-79.1]）和

（95%CI [52.8-68.5]）。3年DSS和LRFS分别为

（

CI [79.490.0]）和

（

CI [82.1-92.0]）。图 1 显示了根据手术切缘距离和 T 状态对 RFS 的 Kaplan-Meier 估计。

Table 3 shows results of univariable analysis of OS and RFS. The following variables were significantly associated with OS and RFS: pathological T-status, N-status, PNI, and adjuvant RT. When adjusting for these four variables in multivariable analysis, the following variables were significantly associated with better OS: deep margin distance

to the proposed threshold (

) and mucosal margin distance as a continuous variable (HR

). A mucosal margin distance

to the proposed threshold only showed a statistical trend for better

.
表 3 显示了 OS 和 RFS 的单变量分析结果。以下变量与 OS 和 RFS 显著相关：病理 T 状态、N 状态、PNI 和辅助 RT。在多变量分析中调整这四个变量时，以下变量与较好的OS显著相关：到建议阈值的深边距

（

）和作为连续变量的粘膜边距（HR

）。与建议阈值的粘膜边缘距离

仅显示出更好的

统计趋势。

TABLE 1 Pathological outcomes.
表1 病理结局。

Pathological data 病理数据	Patients, 病人
Differentiation 分化
Low 低
Medium 中等
High 高
Missing 失踪	2
Tumor size 肿瘤大小

and 和

Missing 失踪	1
Depth of invasion 入侵深度

and 和

Missing 失踪	4
Bone invasion: Yes 骨侵袭：是
Perineural invasion 神经周围浸润
Presence 存在
Yes 是的
Missing 失踪	1
Quantity 数量
Numerous 众多
Rare 罕见
Missing 失踪	45
Lymphovascular emboli ( 淋巴血管栓塞（
Yes 是的
Missing 失踪	2
Worst pattern of invasion 最糟糕的入侵模式
Cohesive 粘性
Non-cohesive 非内聚性
Missing 失踪	176
Distant tumor nodule: Yes 远处肿瘤结节：是
Dysplasia in surrounding tissue: Yes 周围组织发育不良：是
status 地位


pT3 pT3型
pT4 pT4型
status 地位
pNo p否	74 (43.8)
	21

	17 (10.1)

TABLE 1 (Continued) 表1（续）

Pathological data 病理数据	Patients, (%) 患者，（%）



No neck dissection (pNx) 无颈部清扫术（pNx）	54
Extracapsular spread: Yes 包膜外扩散：是
Lymph node ratio 淋巴结比值
(LR) （英国劳氏）
0.025 and (IR) 0.025 和（IR）
(HR) （人力资源）
Missing 失踪	63

Abbreviations: HR, high risk; IR, intermediate risk; LR, low risk.
缩写：HR，高风险;IR，中等风险;LR，低风险。

TABLE 2 Margin distances on histology.
表2 组织学上的切缘距离。

Margin distances 边距距离
Mucosal margin 黏膜边缘
T1/T2 T1/T2 型


Missing 失踪	1



Deep margin 深边距




	8

In multivariable analysis, a deep margin distance

to the proposed threshold remained associated with an improved RFS after adjusting for pathological T-status, N-status, PNI, adjuvant RT, and mucosal margin distance (HR

), as shown in Table 4. A mucosal margin distance

to the proposed threshold was not significantly associated with better RFS in multivariable analysis (

[0.45-1.34];

). When studied as continuous variables in multivariable analysis, the mucosal margin distance (

0.98];

) was significantly associated with RFS
在多变量分析中，在调整病理 T 状态、N 状态、PNI、辅助 RT 和粘膜边缘距离（HR

）后，与拟议阈值的深切缘距离

仍然与改善的 RFS 相关，如表 4 所示。在多变量分析中，

黏膜边缘距离与更好的RFS没有显著相关性（

[0.45-1.34];

）。在多变量分析中作为连续变量进行研究时，粘膜边缘距离（

0.98];

）与RFS显著相关

FIG U RE 1 Recurrence-free survival (RFS) using Kaplan-Meier method according to surgical margin distance and T-status. [Color figure can be viewed at wileyonlinelibrary.com]
图 1 根据 Kaplan-Meier 方法根据手术切缘距离和 T 状态的无复发生存期（RFS）。[彩色图可在 wileyonlinelibrary.com 查看]

and the deep margin distance showed a statistical trend (HR

).
较深边距呈现统计趋势（HR

）。

Figure 2 displays the decision curves at 2 years for the deep and mucosal margins, showing the net benefit of the margins on the RFS at 2 years for T1-T2 and T3-T4 tumors (clinical usefulness). In 2-year RFS prediction for T1-T2 tumors, when the threshold probability was between

and

, the net benefits of the deep margins were better than the scenes when all patients recurred/died or none; and when the threshold probability was between

and

, close observations were found for mucosal margins. For T3-T4 tumors, when the threshold probability was between

and

, the net benefit of the deep margins (but not the mucosal margins) were slightly better than the scenes when all patients recurred/died or none. For T1-T2 tumors, the net benefits of the deep margin were higher than those of the mucosal margin while they were relatively close similar for T3-T4 tumors. A similar observation was made for 1-year RFS prediction (Data S1, Supporting Information).
图 2 显示了深部和粘膜边缘 2 年的决策曲线，显示了 2 年时 RFS 边缘对 T1-T2 和 T3-T4 肿瘤的净益处（临床有用性）。在 T1-T2 肿瘤的 2 年 RFS 预测中，当阈值概率介于和

之间

时，深切缘的净收益优于所有患者复发/死亡或无复发的场景;当阈值概率介于

和

之间时，发现粘膜边缘的观察结果接近。对于 T3-T4 肿瘤，当阈值概率介于

和

之间时，深切缘（但不是黏膜切缘）的净获益略优于所有患者复发/死亡或无复发的场景。对于 T1-T2 肿瘤，深缘的净获益高于黏膜边缘的净获益，而 T3-T4 肿瘤的净获益相对接近。对 1 年 RFS 预测（数据 S1，支持信息）也进行了类似的观察。

Of note, a total of 73 patients with a T1-T2 tongue SCC without adverse pathological features did not receive adjuvant therapy as per multidisciplinary meeting recommendation. Among them, 11 (

) presented with a recurrence, that is, 9 local recurrences, 1 nodal recurrence and 1 distant metastasis. The number of events did not allow to perform relevant statistical analyses of risk factors for recurrence.
值得注意的是，共有 73 例无不良病理特征的 T1-T2 舌鳞状细胞癌患者未按照多学科会议建议接受辅助治疗。其中，11例（

）出现复发，即局部复发9例，淋巴结复发1例，远处转移1例。事件的数量不允许对复发的危险因素进行相关的统计分析。

4 | DISCUSSION 4 |讨论

In this study of 223 patients treated surgically for a primary oral tongue SCC and followed for a median duration of 37.5 months (

CI [34.3-42.8]), we observed a 5 -year OS and RFS of

(95%CI [63.7-79.1]) and

(

CI [52.8-68.5]), respectively. We assessed the influence of surgical margin distance on survival, with a focus on a proposed clinically applicable threshold inspired by the existing literature,

that is,

for both mucosal and deep margins in T1-T2 tumors, and

for both mucosal and deep margins in T3-T4 tumors. Interestingly, RFS of patients with T1-T2 tumors and mucosal or deep margins

was comparable or worse than that of patients with T3-T4 tumors and mucosal or deep margins

(Figure 1). This highlights the prognostic importance of resection margins.
在这项研究中，我们观察到223例原发性口腔舌鳞状细胞癌手术治疗患者，中位随访时间为37.5个月（

CI [34.3-42.8]），我们观察到5年OS和RFS分别为

（95%CI [63.7-79.1]）和

（

CI [52.8-68.5]）。我们评估了手术切缘距离对生存率的影响，重点关注受现有文献启发的临床适用阈值，

即

T1-T2 肿瘤的粘膜和深缘，以及

T3-T4 肿瘤的粘膜和深缘。有趣的是，T1-T2 肿瘤和粘膜或深缘患者的 RFS 与 T3-T4 肿瘤和粘膜或深缘

患者相当或更差

（图 1）。这凸显了切除切缘的预后重要性。

However, the optimal surgical margin threshold is still a matter of debate. The Royal College of Pathologists has defined surgical margins as follows:

as involved,

as close, and

as clear.

The most recent meta-analysis studying surgical margin distances by the millimeter in oral cavity cancers reported that the risks ratios for local recurrence gradually decreased as the margins increased, with a plateau at

Several studies focused on oral tongue cancers, generally reporting outcomes for the

threshold.

The available literature often does not distinguish mucosal margins from deep margins, and never adjusts the threshold according to tumor-related factors that may influence the risk of recurrence.

Indeed, advanced tumors may require larger excision margins as they are more likely to exhibit a noncohesive invasion pattern, PNI, LVE, or tumor satellites.

然而，最佳手术切缘阈值仍然是一个有争议的问题。英国皇家病理学家学会（Royal College of Pathologists）对手术切缘的定义如下：

受累、

接近和

清晰。

最近一项研究口腔癌手术切缘距离（毫米）的荟萃分析报告称，随着切缘的增加，局部复发的风险比逐渐降低，在

几项研究集中在口腔舌癌上，通常报告了

阈值的结果。

现有文献通常不区分黏膜边缘和深层边缘，也从不根据可能影响复发风险的肿瘤相关因素调整阈值。

事实上，晚期肿瘤可能需要更大的切除切缘，因为它们更有可能表现出非粘性侵袭模式、PNI、LVE 或肿瘤卫星。

Multivariable analysis showed that a deep margin distance

to the proposed threshold was associated with a 2.5 -fold better RFS (

[0.23-0.70];

) and OS (HR

[0.19-0.69];

. On the other
多变量分析显示，与建议阈值的较深边际距离

与2.5倍的RFS相关（

[0.23-0.70];

）和OS（HR

[0.19-0.69];

。另一方面

TABLE 3 Univariable analysis of overall survival (OS) and recurrence-free survival (RFS).
表3 总生存期（OS）和无复发生存期（RFS）的单变量分析。

Note: Statistically significant

-values are highlighted in bold; statistical trends are highlighted in italic.
注意：具有统计显著性的

-值以粗体突出显示;统计趋势以斜体突出显示。

Abbreviations: CI, confidence interval; HR, hazard ratio; OS, overall survival; RFS, recurrence-free survival.
缩写：CI，置信区间;HR，风险比;OS，总生存期;RFS，无复发生存期。

Threshold

for

tumors,

for

tumors. The threshold is identical for mucosal and deep margins.

肿瘤的阈值，

肿瘤

的阈值

。黏膜边缘和深边缘的阈值相同。
hand, a mucosal margin distance

to the proposed threshold seemed to have a more limited prognostic significance for

[0.31-1.08];

and RFS (HR

[0.45-1.34];

in multivariable analysis. Of note, due to a lower number of events for OS, a different statistical model was performed for the multivariable analysis of OS (independent model for each
手部，黏膜边缘距离到建议阈值的预后意义

似乎更有限[0.31-1.08];

和 RFS （HR

[0.45-1.34];

在多变量分析中。值得注意的是，由于 OS 的事件数量较少，因此对 OS 的多变量分析执行了不同的统计模型（每个独立模型

TABLE 4 Multivariable analysis of recurrence-free survival.
表4 无复发生存期的多变量分析。

		-value -价值
pT-status pT状态
	1.00
		0.424
-status -地位
	1.00
		0.036
Adjuvant radiotherapy 辅助放疗
No 不	1.00
Yes 是的		0.528
Perineural invasions 神经周围浸润
No 不	1.00
Yes 是的		0.469
Mucosal margins 黏膜边缘
Threshold 门槛	1.00
Threshold 门槛		0.367
Deep margins 深边距
Threshold 门槛	1.00
Threshold 门槛		0.001

Note: Statistically significant

-values are highlighted in bold.
注意：具有统计显著性的

值以粗体突出显示。

Threshold

for T1/T2 tumors,

for T3/T4 tumors. The threshold is identical for mucosal and deep margins.

T1/T2 肿瘤的阈值，

T3/T4 肿瘤的阈值

。黏膜边缘和深边缘的阈值相同。

margin, i.e., mucosal and deep) and RFS (one global model including mucosal and deep margins).
边缘，即粘膜和深部）和 RFS（一个包括粘膜和深部边缘的全局模型）。

The decision curve analysis is complementary to the survival analyses. It combines benefits and harms to evaluate the overall net benefit of a predictive factor.

To the best of our knowledge, there is no literature utilizing this innovative method to assess the net benefit of predictive factors in head and neck oncology. In this article, the decision curve analysis indicated that mucosal and deep margin distances were globally clinically useful for the 1and 2-year RFS prediction of T1-T2 tumors, although deep margins seemed to have more clinical utility than mucosal margins (Figure 2).
决策曲线分析是对生存分析的补充。它结合了益处和危害来评估预测因素的总体净收益。

据我们所知，没有文献利用这种创新方法来评估预测因素在头颈部肿瘤学中的净益处。在本文中，决策曲线分析表明，粘膜和深缘距离对于 T1-T2 肿瘤的 1 年和 2 年 RFS 预测具有整体临床意义，尽管深缘似乎比粘膜边缘更具临床效用（图 2）。

The decision curve analysis also showed that the influence of margin distances on 2-year RFS seemed greater for T1-T2 tumors than T3-T4 tumors, suggesting that the prognosis of more advanced tumors may be more driven by other adverse prognostic factors, for example,

-status, tumor differentiation, PNI, LVE. Nevertheless, this could not be confirmed by subgroup multivariable analysis given the low number of events in T1-T2 tumors.
决策曲线分析还显示，T1-T2肿瘤的切缘距离对2年RFS的影响似乎大于T3-T4肿瘤，这表明更晚期肿瘤的预后可能更多地受其他不良预后因素的驱动，例如

状态、肿瘤分化、PNI、LVE。然而，鉴于 T1-T2 肿瘤中的事件数量较少，这无法通过亚组多变量分析证实。

In their study of 151 patients comprising mainly early-stage oral tongue SCC (74.2% of T1-T2 tumors), Lee et al. proposed different margin distance thresholds for nearest mucosal and deep margins, ranging from 2.5 to

. These cut-off values varied according to T-status (T1-T2 vs. T3-T4) and on the type of event: local recurrence, overall recurrence, survival.

However, the statistical method used to determine such cut-off is not sufficiently detailed to properly assess its validity. Besides, their low number of advanced T-status (39 T3-T4 tumors) makes their inference about advanced tumors hazardous. Finally, the multiplicity of the thresholds they found ( 36 in total) and the precision of their values (

) make it inapplicable, similarly to the study by
在对 151 名主要包括早期口腔舌鳞状细胞癌（占 T1-T2 肿瘤的 74.2%）的患者的研究中，Lee 等人提出了最近粘膜和深缘的不同边缘距离阈值，范围从 2.5 到

。这些临界值根据 T 状态（T1-T2 与 T3-T4）和事件类型而变化：局部复发、总体复发、生存率。

然而，用于确定这种临界值的统计方法不够详细，无法正确评估其有效性。此外，他们的晚期 T 状态数量很少（39 个 T3-T4 肿瘤）使他们对晚期肿瘤的推断变得危险。最后，他们发现的阈值（总共 36 个）的多重性和其值的精度（

）使其不适用，类似于

FIGURE 2 Decision curves showing the net benefit of the deep and mucosal margin distances on recurrence-free survival (RFS) at 24 months for

and

tumors. [Color figure can be viewed at wileyonlinelibrary.com]
图 2 决策曲线显示了深部和粘膜边缘距离对

肿瘤 24 个月

时无复发生存期（RFS）的净益处。[彩色图可在 wileyonlinelibrary.com 查看]

Otsuru et al.

In our study, we assessed a clinically applicable surgical margin threshold that varied according to T-status, and only the deep margin threshold was independently associated with RFS. This suggests that a shorter deep margin distance may be aimed for in

versus T3-T4 tumors.
Otsuru 等人。

在我们的研究中，我们评估了临床上适用的手术切缘阈值，该阈值根据 T 状态而变化，只有深切缘阈值与 RFS 独立相关。这表明

，与 T3-T4 肿瘤相比，更短的深切缘距离可能更短。

Among the study limitations are its retrospective nature and the numerous factors that may interfere with the interpretation of margin quality. They include the thermal injury of margins

and the tissue shrinkage, which varies depending on tissue properties and anatomic location.

They also comprise the sampling error inherent to all pathological examinations,

the consideration of the intraoperative harvesting of margins, and the non-consensual definition of what a positive margin is, especially regarding carcinoma in situ and margins

Finally, survival data must be interpreted with caution as the date of surgery (and not of radiotherapy completion, when performed) was used to assess survival. The strengths of this single-center study are the rarity of missing data, the consistency of pathological analysis and reporting as well as its strict inclusion criteria. Focusing only on oral tongue limited the number of included patients, but allowed a more homogeneous comparison of cases, resulting in more meaningful conclusions.
研究的局限性包括其回顾性以及可能干扰边际质量解释的众多因素。它们包括边缘的热损伤

和组织收缩，这取决于组织特性和解剖位置。

它们还包括所有病理检查固有的抽样误差、

术中切缘采集的考虑以及对什么是阳性切缘的非同意定义，尤其是关于原位癌和切缘

。

最后，生存数据必须谨慎解释，因为手术日期（而不是放疗完成时）用于评估生存率。这项单中心研究的优势在于缺失数据的稀有性、病理分析和报告的一致性以及严格的纳入标准。仅关注口腔舌限制了纳入的患者数量，但允许对病例进行更同质的比较，从而得出更有意义的结论。

5 | CONCLUSION 5 |结论

In this single-center retrospective study of oral tongue SCC, mucosal and deep margin distances were both associated with OS and RFS. The influence of margin distances on RFS seemed greater for T1-T2 tumors than T3-T4 tumors, suggesting that the prognosis of more advanced tumors may be more driven by other adverse prognostic factors.
在这项口腔舌鳞状细胞癌的单中心回顾性研究中，粘膜和深缘距离都与 OS 和 RFS 相关。T1-T2 肿瘤的切缘距离对 RFS 的影响似乎大于 T3-T4 肿瘤，这表明更晚期肿瘤的预后可能更多地受其他不良预后因素的驱动。

Finally, we assessed a clinically applicable surgical margin threshold that varied according to

-status, and unlike for mucosal margins, the deep margin threshold was significantly associated with RFS and OS. This indicates that a shorter deep margin distance may therefore be aimed for in T1-T2 versus T3-T4 tumors. These findings warrant external validation by further studies.
最后，我们评估了临床上适用的手术切缘阈值，该阈值因

状态而异，与粘膜边缘不同，深切缘阈值与RFS和OS显著相关。这表明，因此，与 T3-T4 肿瘤相比，T1-T2 的深切缘距离可能更短。这些发现值得进一步研究的外部验证。

ACKNOWLEDGMENT 确认

The authors want to thank Morgane Marcou for her administrative support.
作者要感谢Morgane Marcou的行政支持。

CONFLICT OF INTEREST STATEMENT
利益冲突声明

The authors declare no conflicts of interest.
作者声明没有利益冲突。

DATA AVAILABILITY STATEMENT
数据可用性声明

The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions
支持本研究结果的数据可应通讯作者的要求提供。由于隐私或道德限制，这些数据不公开

ETHICS STATEMENT 道德声明

A declaration to the National Commission on Informatics and Liberty (CNIL) was made in accordance with the General Data Protection Regulation Articles 15-20 under the reference F20230315180652. The study was conducted in compliance with the Helsinki Declaration.
根据《通用数据保护条例》第 15-20 条在参考F20230315180652下向国家信息学和自由委员会（CNIL）发表声明。这项研究是根据《赫尔辛基宣言》进行的。

ORCID

Valentine Poissonnet (D) https://orcid.org/0000-0001-66760916
瓦伦丁泊松内（D） https://orcid.org/0000-0001-66760916

Franck Delanoë (1) https://orcid.org/0000-0002-1001-9827
Franck Delanoë （1） https://orcid.org/0000-0002-1001-9827

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SUPPORTING INFORMATION 支持信息

Additional supporting information can be found online in the Supporting Information section at the end of this article.How to cite this article: Poissonnet V, Segier B,
其他支持信息可在本文末尾的“支持信息”部分在线找到。如何引用本文： Poissonnet V， Segier B，
Lopez R, et al. Prognostic implications of mucosal
Lopez R 等人。黏膜的预后意义
and deep margin distances according to T-status in
和根据 T 状态的深边距
oral tongue squamous cell carcinoma: A single-
口腔舌鳞状细胞癌：单
center retrospective study. Head & Neck. 2024;1-9.
中心回顾性研究。头部和颈部。2024;1-9.
doi:10.1002/hed.27844 doi：10.1002/hed.27844

How to cite this article: Poissonnet V, Segier B, Lopez R, et al. Prognostic implications of mucosal and deep margin distances according to T-status in oral tongue squamous cell carcinoma: A singlecenter retrospective study. Head & Neck. 2024;1-9. doi:10.1002/hed.27844
引用本文： Poissonnet V， Segier B， Lopez R， et al.口腔舌鳞状细胞癌根据 T 状态的粘膜和深缘距离的预后影响：一项单中心回顾性研究。头部和颈部。2024;1-9.doi：10.1002/hed.27844

Prognostic implications of mucosal and deep margin distances according to -status in oral tongue squamous cell carcinoma: A single-center retrospective study 根据 口腔舌鳞状细胞癌状态的粘膜和深缘距离的预后影响：一项单中心回顾性研究

Correspondence 通信

Abstract 抽象

KEYWORDS 关键字

1 | INTRODUCTION 1 |介绍

2 | MATERIALS AND METHODS2 |材料与方法

2.1 | Statistical analysis2.1 |统计分析

3 | RESULTS 3 |结果

4 | DISCUSSION 4 |讨论

5 | CONCLUSION 5 |结论

ACKNOWLEDGMENT 确认

CONFLICT OF INTEREST STATEMENT利益冲突声明

DATA AVAILABILITY STATEMENT数据可用性声明

ETHICS STATEMENT 道德声明

ORCID

REFERENCES 引用

SUPPORTING INFORMATION 支持信息

Prognostic implications of mucosal and deep margin distances according to -status in oral tongue squamous cell carcinoma: A single-center retrospective study
根据口腔舌鳞状细胞癌状态的粘膜和深缘距离的预后影响：一项单中心回顾性研究

2 | MATERIALS AND METHODS
2 |材料与方法

2.1 | Statistical analysis
2.1 |统计分析

CONFLICT OF INTEREST STATEMENT
利益冲突声明

DATA AVAILABILITY STATEMENT
数据可用性声明