J Stomatol Oral Maxillofac Surg 118 (2017) 84–89

Available online at

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Original Article

Oral cancer characteristics in France: Descriptive epidemiology for

early detection
K. Jéhannin-Ligier a,*, O. Dejardin b, B. Lapôtre-Ledoux h, S. Bara e, G. Coureau f,
P. Grosclaude g, E. Marrer i, F. Molinié j, B. Trétarre k, M. Velten l,
A.-S. Woronoff m, M. Colonna c, A.V. Guizard d
a
General Cancer Registry of Lille and its area, GCS-C2RC, 59037 Lille, France
b
University Hospital of Caen, U1086 Inserm UCBN ‘‘Cancers & preventions’’, 14000 Caen, France
c
General Cancer Registry of Isère, University Hospital of Grenoble, 38000 Grenoble, France
d
General Tumour Registry of Calvados, Centre F.-Baclesse, 14000 Caen, France
e
Registre des cancers de la Manche, 50100 Cherbourg, France
f
Registre de cancer de Gironde, 33000 Bordeaux, France
g
Registre des cancers du Tarn, 81000 Albi, France
h
Registre du cancer de la Somme, 80000 Amiens, France
i
Registre des cancers du Haut-Rhin, 68100 Mulhouse, France
j
Registre des tumeurs de Loire-Atlantique et Vendée, 44000 Nantes, France
k
Registre des tumeurs de l’Hérault, 34000 Montpellier, France
l
Registre des cancers du Bas-Rhin, 67000 Strasbourg, France
m
Registre des tumeurs du Doubs et du Territoire de Belfort, 25000 Besançon, France

A R T I C L E I N F O A B S T R A C T

Article history: Despite the frequency and lethality of oral cancers in France, there are no detailed general population
Received 29 November 2016 data regarding the characteristics of these patients to fuel the public health authorities’ reflections about
Accepted 15 February 2017 early detection policies. Thus, the objective of this study was to determine, in the general population, the
Available online 24 February 2017
characteristics of both patients and tumours at the time of the diagnosis. A high-resolution, population-
based study using 13 French registries was conducted on 1089 tumours diagnosed in 2010. Men
Keywords: accounted for 75% of cases. The most frequent sites were tonsil (28.4%) and oral tongue (21.1%). The
Oral cavity cancer
median age varied from 56.7 years for floor of mouth to 66.4 years for gum. The lesions were mainly
Population-based study
Stage at diagnosis
diagnosed on pain and those diagnosed after routine clinical examination were scarce (2.6%). There were
Early detection 65.5% stage III and IV at diagnosis. Oral tongue, floor of mouth and palate presented tumours less than
2 cm only in 34 to 40% of cases. Advanced stage was associated with the presence of comorbidities, and
tonsil or base of tongue topography. Stage was not associated with Département, deprivation index or
gender. This study provided a picture of the characteristics of oral cancer patients and their tumours and
showed that diagnoses are often made late, even for those tumours most easily accessible to direct visual
and tactile examination. Nevertheless, it remains to define the target population of an early detection
and to evaluate the benefit of such detection on the mortality rate.
C 2017 Elsevier Masson SAS. All rights reserved.

1. Introduction
In Europe, oral cavity and pharynx cancers are the sixth most
common group of cancers among men with an estimated annual
incidence of 73,900 cases and 34,200 deaths [1]. France has an
incidence rate amongst the highest in Europe [1], although it is
* Corresponding author. Registre général des cancers de Lille et de sa région,
C2RC, Pavillon Breton, Hôpital Calmette, CHRU de Lille, boulevard du Professeur-
Jules-Leclercq, 59037 Lille cedex, France.
E-mail address: kligier@registrecancers59.fr (K. Jéhannin-Ligier).
constantly decreasing [2]; there were an estimated 4384 new cases
of oral and oropharynx cancer in men and 2117 in women in 2010
[3].
The main risk factors are tobacco and alcohol [4], consump-
tion of which explains 82.9% of cases [5]. In the last
decade, human papillomavirus has been recognized as a
carcinogenic agent for oropharynx [6]. In addition, these cancers
are strongly linked to socioeconomic factors: the risk of
developing an oral cancer is greater in those with a low level
of education or a low income, regardless of smoking or alcohol
consumption [7].

http://dx.doi.org/10.1016/j.jormas.2017.02.003
2468-7855/ C 2017 Elsevier Masson SAS. All rights reserved.
 K. Jéhannin-Ligier et al. / J Stomatol Oral Maxillofac Surg 118 (2017) 84–89 85

The prognosis of oral cavity and oropharynx cancers is extremely
poor in France, with a 5-year net survival of 43% and 37%, and a 10-
year net survival of 28% and 19%, respectively [8]. This figure is
amongst the lowest of European countries [9] and has hardly
improved over the last 15 years. The major determinant of this
lower survival rate is the stage at diagnosis: 5-year survival in
patients diagnosed at an advanced stage is reduced by a factor of
1.5 to 2 compared with that for patients diagnosed at a localised
stage [9]. On top of this, aggressive treatment regimes following late
diagnosis can lead to serious sequels that affect quality of life [10].
Given the high incidence and poor prognosis, the screening or
early detection of these cancers, easily accessible on visual
inspection and manual palpation, is a public health issue in many
countries [11]. Thus, the French governmental cancer plan 2009–
2013 [12] advocated early detection of oral cavity cancers.
Following this, the National Cancer Institute (INCa) set up
multimedia training for dentists (2009) and general practitioners
(2010) to teach them how to detect suspicious lesions through an
in-depth examination of the oral cavity in high-risk patients
[13]. Despite the frequency and lethality of these cancers, there are
no detailed French general population data regarding the charac-
teristics of these patients to fuel the public health authorities’
reflections about early detection policies. Thus, the objective of this
study was to determine, in the general population, the characte-
ristics of the patients and their tumours at the time of diagnosis.
2. Material and methods
2.1. Population
This high-resolution, population-based study concerned all
patients aged over 20 years with a diagnosis of invasive oral cancer
in 2010. Tumours were categorised according to the International
Classification of Diseases for Oncology – third edition – ICD-O 3 as:

Table 1
Characteristics of patients with incident oral cancer in France (2010) and univariate analysis of tumour stage at diagnosis.

Stage I–II Stage III–IV P univariate Total

(n = 1089)

Variable n % n % n %

Sex 0.03
Male 213 27.4 564 72.6 817 75.0
Female 87 34.4 166 65.6 272 25.0
Age 0.03
< 55 111 31.4 242 68.6 369 33.9
[55–65[ 92 24.2 289 75.8 395 36.3
 65 97 32.8 199 67.2 325 29.8
Département 0.36
Calvados 26 33.3 5 66.7 81 7.4
Doubs 18 32.1 38 67.9 58 5.3
Gironde 37 31.9 79 68.1 122 11.2
Hérault 21 25.9 60 74.1 86 7.9
Isère 36 35.3 66 64.7 104 9.5
Loire-Atlantique 30 22.6 103 77.4 148 13.6
Manche 20 37.7 33 62.3 54 5.0
Lille et sa région 36 31.9 77 68.1 115 10.6
Bas-Rhin 23 29.1 56 70.9 88 8.1
Haut-Rhin 14 26.9 38 73.1 54 5.0
Somme 20 24.7 61 75.3 83 7.6
Tarn 9 30.0 21 70.0 32 2.9
Vendée 10 17.9 46 82.1 64 5.9
Deprivation quintile 0.68
Privileged 1 54 31.2 119 68.8 186 17.1
Quite privileged 2 48 27.8 125 72.2 180 16.5
Quite underprivileged 3 48 26.2 135 73.8 195 17.9
Underprivileged 4 75 32.2 158 67.8 245 22.5
Very underprivileged 5 75 28.7 186 71.3 276 25.3
Unknown 7 0.6
Age-adjusted Charlson comorbidity index 0.01
0 56 39.4 86 60.6 146 13.4
1–2 131 26.6 362 73.4 510 46.8
3 111 28.3 281 71.7 426 39.1
Unknown 7 0.7
Tumour site < 0.001
C01: base of tongue 6 4.8 118 95.2 125 11.5
C02: oral tongue 121 57.9 88 42.1 230 21.1
C03: gum 17 23.0 57 77.0 78 7.2
C04: floor of mouth 48 35.6 87 64.4 148 13.6
C05: palate 46 41.8 64 58.2 118 10.8
C06: other & unspecified parts of mouth 21 29.2 51 70.8 81 7.4
C09: tonsil 41 13.4 265 86.6 309 28.4
Mode of discovery
Pain 170 34.2 327 65.8 525 48.2
Dyspnea 3 42.7 4 57.1 8 0.7
Dysphonia 6 28.6 15 71.4 21 1.9
Oral bleeding 4 28.6 10 71.4 16 1.5
Cervical swelling 30 13.2 197 86.8 230 21.1
Impaired general status 9 8.3 99 91.7 111 10.2
Clinical exam without symptoms 17 65.4 9 34.6 28 2.6
Fortuitous 12 34.3 23 65.7 39 3.6
Unknown 111 10.2
86 K. Jéhannin-Ligier et al. / J Stomatol Oral Maxillofac Surg 118 (2017) 84–89
base of tongue (C01), oral tongue (C02), gum (C03), floor of mouth
(C04), palate (C05), cheek mucosa, vestibule and retromolar area
(C06), tonsil and glossotonsillar sulcus (C09). Lymphomas,
sarcomas and patients with a history of invasive or in situ cancer
(except basal or squamous cell carcinoma of the skin) were
excluded from the study. In total, 1089 tumours were included
(Table 1).
Patients included in the study were taken from 13 population-
based cancer registries (Calvados, Doubs, Gironde, Hérault, Isère,
Loire-Atlantique, Manche, Zone de proximité de Lille, Haut-Rhin,
Bas-Rhin, Somme, Tarn, Vendée), which cover 18% of the French
population. The completeness and data quality of these registries
are regularly assessed by the International Agency for Research on
Cancer (IARC) or by the European Network of Cancer Registries
(ENCR).
2.2. Data
Thanks to a specific survey, high-resolution data were collected
from medical records and concerned identity details, place of
residence, comorbidities, date of diagnosis, topography and
morphology of cancer (ICD-O 3), circumstances of discovery and
clinical stage (UICC/AJCC TNM seventh edition).
For coding of metastatic spread, the minimum examination
required was a thoracic examination (radiography associated with
bronchoscopy or CT scan or PET). Without this examination, M
stage was coded 0 for patients who did not undergo chemotherapy
and had no metastatic evolution at 2 years.
As there is no individual socioeconomic data in the medical
records, the socioeconomic status of patients was evaluated by
measuring that of their place of residence at diagnosis using a
social deprivation index, the EDI [14]. In our statistical analyses, we
used the national quintiles of this index.
2.3. Data analysis
The age-adjusted Charlson comorbidity index (ACCI) [15]
was calculated and categorized into three classes: 0 (no
comorbidity), 1–2 (moderate comorbidities), and 3 (severe
comorbidities).
We tested associations between qualitative variables using the
Chi2 test or Fisher’s exact test. Quantitative variables were
described by median and 25th and 75th percentiles (Q1–Q3).
Comparisons between medians were performed using the
Kruskall–Wallis test.
To ascertain the determinants of advanced stage at
diagnosis, logistic regression was used to calculate the adjusted
odds ratio (ORa) with a 95% confidence interval (95% CI) of early
stage (stages I–II) versus advanced stage (stages III–IV) of
disease. The models included only cases with no missing values
for the variables studied. For the logistic regression, the
topographies of the cancers were divided into 2 groups
according to the ease of clinical inspection: C02 to C06 (oral
tongue, gum, floor of mouth, palate, mouth) versus C01 and C09
(base of tongue and tonsil).
To investigate specifically the influence of age and of
comorbidities, logistic regression models were performed. Thus,
gender, Département, deprivation quintile and topography of
cancer were entered into model-1. Model-2 was based on
model-1 plus the age at diagnosis in three categories (< 55;
[55–65[;  65). Model-3 was based on model-1 plus the Charlson
score (i.e. comorbidities only, regardless of age). Model-4 was
based on model-1 plus the ACCI.
Analyses were conducted using StataIC 13 software
(StataCorp. Stata: Statistical Software Release 13 College Station.
TX. StataCorp LP).
3. Results
3.1. Characteristics of patients and tumours
The median age at diagnosis was 58.7 years (Q1: 52.5–Q3:
67.6). Seventy-five per cent of the patients were male and 53.2%
fell into the age groups between 50 and 64 years (Fig. 1). Almost
half of the patients belonged to the deprivation quintile
‘‘underprivileged’’ or ‘‘very underprivileged’’ and more than a
third had severe comorbidities at diagnosis (Table 1). The most
frequent sites were tonsil (28.4%) and oral tongue (21.1%).
Distribution by site was different depending on sex (P < 0.001):
the topographies gum and oral tongue were more frequent among
women; floor of mouth and base of tongue were more frequent
among men. The median age differed according to site, ranging
from 56.7 years [Q1: 51.0–Q3: 62.7] for floor of mouth tumours to
66.4 years for gum tumours [Q1: 55.6–Q3: 83.7] (P < 0.001).
3.2. Mode of discovery
The lesions were mainly diagnosed on pain and nearly a third of
patients had clinically visible cervical swelling or general
impairment (Table 1). Tumours diagnosed after routine clinical
examinations without symptoms were scarce (2.6%), involving oral
tongue, floor of mouth and palate in 67.9% of cases.
3.3. Stage
Locally advanced tumours (cT3–4) accounted for 37.7% of cases
(Table 2). More than half of the cases had at least one clinically
apparent lymph node at diagnosis (58.3%) but there were few
distant metastases (M1 = 5.8%).
The majority of lesions were diagnosed at an advanced clinical
stage (stage IV = 54.4%), (Table 3). There were 50.0% stage I lesions
among tumours detected during clinical examinations in the
absence of specific symptoms.
By anatomic subcategories, lesions diagnosed the latest were
those of the base of tongue (stage IV = 84.0%). Tumours diagnosed
the earliest were those of oral tongue (stage I = 33.5%).
In univariate analysis (Table 1), stage at diagnosis was
associated with sex (P = 0.03), age at diagnosis (P = 0.03), ACCI
(P = 0.01) and tumour site (P < 0.001).
In the multivariate analysis, stage at diagnosis was unrelated to
gender, Département and deprivation quintile but was associated
with tumour location (P < 0.001) (model-1). After adjusting for
these variables, age (model-2) and the Charlson score (i.e.
comorbidities only, regardless of age – model-3) were not
associated with stage.
In model-4, stage was linked to the ACCI (P = 0.009) and to
tumour location (P < 0.001) (Table 4). The stage was more
Fig. 1. Number of incident oral cancers by age group, France, 2010.
 K. Jéhannin-Ligier et al. / J Stomatol Oral Maxillofac Surg 118 (2017) 84–89 87

Table 2
Extent of the oral cancer, presence of regional lymph node metastasis, presence of distant metastasis by subsite, France – 2010.

Topography cT1 cT2 cT3–4 cN 1–3 M1

( 2 cm) (> 2 cm and  4 cm) (> 4 cm or invasion through bone, muscle. . .) (%) (%)
(%) (%) (%)

C01: base of tongue 20 22 78 109 17

(16.0%) (17.6%) (62.4%) (87.2%) (13.6%)
C02: oral tongue 93 69 49 78 9
(40.4%) (30.0%) (21.3%) (33.9%) (3.9%)
C03: gum 10 14 50 37 3
(12.8%) (17.9%) (64.1%) (47.4%) (3.8%)
C04: floor of mouth 51 32 50 76 8
(34.5%) (21.6%) (33.8%) (51.4%) (5.4%)
C05: palate 42 32 31 53 6
(35.6%) (27.1%) (26.3%) (44.9%) (5.1%)
C06: other & unspecified parts of mouth 18 22 35 41 1
(22.2%) (27.2%) (43.2%) (50.6%) (1.2%)
C09: tonsil 55 95 118 241 19
(17.8%) (30.7%) (38.2%) (78.0%) (6.1%)
Total 289 286 411 635 63
(26.5%) (26.3%) (37.7%) (58.3%) (5.8%)

Table 3
Stage at diagnosis according to the topography of the oral cancer, France – 2010.

Topography I II III IV Unknown Total

n % n % n % n % n %

C01: base of tongue 4 3.2 2 1.6 10 8.0 105 84.0 4 3.2 125
C02: oral tongue 77 33.5 44 19.1 24 10.4 63 27.4 22 9.6 230
C03: gum 6 7.7 11 14.1 4 5.1 52 66.7 5 6.4 78
C04: floor of mouth 33 22.3 15 10.1 15 10.1 70 47.3 15 10.1 148
C05: palate 30 25.4 16 13.6 13 11.0 49 41.5 10 8.5 118
C06: other & unspecified parts of mouth 9 11.1 12 14.8 5 6.2 44 54.3 11 13.6 81
C09: tonsil 16 5.2 25 8.1 50 16.2 209 67.6 9 2.9 309
Total 175 16.1 125 11.5 121 11.1 592 54.4 76 7.0 1089

Table 4 advanced for patients with moderate [ORa = 1.86 (95% CI: 1.20–
Determinants of advanced stage at diagnosis for oral cancer in France – 2010.
2.88)] or severe comorbidities [ORa = 1.96 (95% CI: 1.25–3.07)]. It
Multivariate analyse (n = 1020).
was less advanced for cancer topographies oral tongue, gum, floor
Variable ORa 95% CI P-value of mouth, palate, mouth ‘‘C02–C06’’ [ORa = 0.16 (95% CI: 0.11–
Sex 0.24 0.23)] than for base of tongue and tonsil ‘‘C01 and C09’’
Male 1 topography.
Female 0.82 0.59–1.14
Département 0.22
4. Discussion
Somme 1
Calvados 0.6 0.28–1.27
Doubs 0.62 0.27–1.42 This is the first high-resolution, population-based study on the
Gironde 0.68 0.34–1.35 characteristics of oral cavity cancers in France. Our results show
Hérault 0.83 0.39–1.78 that oral cavity cancers were diagnosed late when patients
Isère 0.57 0.28–1.15
presented with symptoms, which were severe in nearly a third
Loire-Atlantique 1.05 0.51–2.13
Manche 0.52 0.23–1.18 of cases. They were discovered among patients aged 50–64 years
Lille et sa région 0.55 0.27–1.09 and coming from deprived areas in nearly half of cases. There was
Bas-Rhin 0.75 0.35–1.60 also a high percentage of comorbidities, possibly related to risk
Haut-Rhin 0.74 0.31–1.73
factors for these tumours. Logistic regression showed that stage
Tarn 0.96 0.32–2.83
Vendée 1.83 0.74–4.57
was not associated with age only or comorbidities only but the
Deprivation quintile 0.94 association existed with the interaction comorbidities-age inte-
Privileged 1 1 grated in the ACCI.
Quite privileged 2 0.85 0.51–1.42 These cancers, which may be discovered by mere visual
Quite underprivileged 3 1.02 0.61–1.69
inspection, are diagnosed at an advanced stage. Compared to
Underprivileged 4 0.89 0.56–1.42
Very underprivileged 5 0.99 0.62–1.58 the Eurocare study [9], the localised stage is diagnosed less
Age-adjusted Charlson 0.009 frequently in France than in some European countries for oral
comorbidity index cavity (C03–C06), 33% vs. 39%, and slightly less frequently for
0 1
oropharynx and tonsil (C09–C10), 17% vs. 19%.
1–2 1.86 1.20–2.88
3 1.96 1.25–3.07
In France, the highest incidences are observed in Départements
Tumour site < 0.001 located in the northern half of France [3], which might suggest a
C01 and C09 1 heterogeneity in stage at diagnosis. However, our study showed
C02 to C06 0.16 0.11–0.23 that the stage at diagnosis is homogeneous throughout the
ORa: adjusted odds ratio; 95% CI: 95% confidence interval; C01 and C09: base of national territory. The distribution of stage showed that only a
tongue and tonsil; C02 to C06: oral tongue, gum, floor of mouth, palate, mouth. quarter of tumours are diagnosed with a size of less than 2 cm. By
88 K. Jéhannin-Ligier et al. / J Stomatol Oral Maxillofac Surg 118 (2017) 84–89
subcategory, oral tongue, floor of mouth and palate presented
tumours less than 2 cm in 34 to 40% of cases. So, early detection
may increase this percentage, especially for these localizations,
which are the most easily accessible to direct visual and tactile
examination.
Tumours diagnosed after routine clinical examinations were
scarce (2.6%). However, the multimedia training for health
professionals about early diagnosis of oral cavity cancers started
only at the end of 2008 and it may be that we have not yet had
enough time to detect an effect. When routine clinical examination
was applied, the proportion of stage I was higher (50.0%).
Why are advanced stages at diagnosis so frequent? A first
hypothesis is that patients do not have access to care. Our study
shows that almost half of the patients belong to the deprivation
quintiles ‘‘underprivileged’’ and ‘‘very underprivileged’’; thus, the
issue of access to care for this population arises and may suggest a
higher stage at diagnosis in this population if this access is
difficult. Nevertheless, a previous study showed that 86% of
patients had visited a general practitioner in the year before the
diagnosis of cancer of the upper aerodigestive tract and, among
them, 78% visited their general practitioner 3 or more times and
this access to care was not socially determined [16]. Moreover, our
study did not find an association between stage at diagnosis and
deprivation quintile, this result was close to that found in another
study [17].
So, patients do visit health providers, especially since 86% of
patients have comorbidities. However, the presence of comorbi-
dities (in the broadest sense of the age-adjusted Charlson
comorbidity index that integrates comorbidity data and age)
was associated with an advanced stage at diagnosis. Furthermore,
for almost half of patients, pain was the major symptom. This
context of non-specific symptoms and comorbidities in patients
who are already weakened by exposure to tobacco and alcohol may
lead to a delay in the diagnosis. Thus, the patient delay – the
interval time between the appearance of symptoms and the first
presentation to the primary health care provider – may vary from
3.5 to 5.4 months [18]. The referral to a specialist may also be
delayed if the primary health care provider and/or patient focuses
on comorbidities and does not take into account non-specific
symptoms that could lead to early detection of oral cancers.
Another study found similar results involving comorbidities and
advanced stages [19].
This first French study of the general population has covered
only 1/5th of the metropolitan population. The main limitation of
the study is the number of cancer registries allowed in France.
However, these cancer registries are located throughout the French
territory.
The main strength of our study resides in its design based on the
method of ‘high-resolution, population-based study’: data were
collected in a precise and rigorous manner, according standardised
procedures, from the medical files in order to know all the
characteristics of the cancer cases included. Thus, missing values
were scarce. The inclusion of patients from the cancer registries
allowed us to overcome the recruitment bias of hospital studies
and give information on the totality of cancer cases in a given
geographic area.
Our study characterizes patients with cancer of the oral cavity
and therefore brings epidemiological information for early
detection. However, the last review of the literature by the
Cochrane group highlighted the lack of studies that would enable
an assessment of the efficacy and cost of a screening programme
for oral cavity cancers [11]. The early detection implemented in
France is a pro-active attitude to this public health problem.
Nevertheless, the benefit of such early detection on the mortality
rate of oral cancers remains to be shown and the target population
must be defined.
This study provides a picture of the characteristics of the
patients and their oral cancers at the beginning of the early
detection policy for these tumours. Despite the recommendations
for early detection, oral cancers are still diagnosed late in France –
including those tumours, which are easily accessible on clinical
examination – perhaps owing to the profiles of the patients.
Authors’ contribution
KL and AVG conceived the study, participated to its design and
coordination and drafted the manuscript. OD participated to the
design of the study. OD and MC helped in drafting the manuscript.
KL, OD and MC performed the statistical analyses. FRANCIM
provided the data. All authors read and approved the final
manuscript.
Funding
IRESP.
Disclosure of interest
The authors declare that they have no competing interest.
Acknowledgements
We thank the ENT specialists, maxillofacial surgeons, oncolo-
gists, pathologists, doctors of the health insurance funds and
patient administrative databases, the multidisciplinary commit-
tees, the medical secretaries and archivists.
They also thank Mr. Khadim Ndiaye for his participation to the
analysis of data and Mrs. Gillian Cadier for the translation of the
manuscript.
References
[1] Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber
H, et al. Cancer incidence and mortality patterns in Europe: estimates for
40 countries in 2012. Eur J Cancer 2013;49(6):1374–403.
[2] Binder-Foucard F, Belot A, Delafosse P, Remontet L, Woronoff AS, Bossard N.
Estimation nationale de l’incidence et de la mortalité par cancer en France
entre 1980 et 2012. Partie 1 – Tumeurs solides. Saint-Maurice: Institut de
veille sanitaire; 2013. p. 122.
[3] Ligier K, Belot A, Launoy G, Velten M, Delafosse P, Guizard AV, et al. [Epidemi-
ology of oral cavity cancers in France]. Rev Stomatol Chir Maxillofac
2011;112(3):164–71.
[4] Righini CA, Karkas A, Morel N, Soriano E, Reyt E. [Risk factors for cancers of the
oral cavity, pharynx (cavity excluded) and larynx]. Presse Med 2008;37(9):
1229–40.
[5] Radoi L, Menvielle G, Cyr D, Lapotre-Ledoux B, Stucker I, Luce D, et al.
Population attributable risks of oral cavity cancer to behavioral and medical
risk factors in France: results of a large population-based case-control study,
the ICARE study. BMC Cancer 2015;15:827.
[6] Herrero R, Castellsague X, Pawlita M, Lissowska J, Kee F, Balaram P, et al.
Human papillomavirus and oral cancer: the International Agency for Research
on Cancer multicenter study. J Natl Cancer Inst 2003;95(23):1772–83.
[7] Conway DI, Brenner DR, McMahon AD, Macpherson LM, Agudo A,
Ahrens W, et al. Estimating and explaining the effect of education and
income on head and neck cancer risk: INHANCE consortium pooled analysis
of 31 case-control studies from 27 countries. Int J Cancer 2015;136(5):
1125–39.
[8] Grosclaude P, Remontet L, Belot A, Danzon A, Rasamimanana Cerf N, Bossard N.
Survie des personnes atteintes de cancer en France. 1989–2007 – Étude à partir
des registres des cancers du réseau Francim. Saint-Maurice: Institut de veille
sanitaire; 2013.
[9] Gatta G, Botta L, Sanchez MJ, Anderson LA, Pierannunzio D, Licitra L, et al.
Prognoses and improvement for head and neck cancers diagnosed in Europe in
early 2000s: the EUROCARE-5 population-based study. Eur J Cancer 2015;51(15):
2130–43.
[10] Babin E, Sigston E, Hitier M, Dehesdin D, Marie JP, Choussy O. Quality of life in
head and neck cancers patients: predictive factors, functional and psychoso-
cial outcome. Eur Arch Otorhinolaryngol 2008;265(3):265–70.
[11] Brocklehurst P, Kujan O, O’Malley LA, Ogden G, Shepherd S, Glenny AM.
Screening programmes for the early detection and prevention of oral cancer.
Cochrane Database Syst Rev 2013;(11):CD0041.
 K. Jéhannin-Ligier et al. / J Stomatol Oral Maxillofac Surg 118 (2017) 84–89
[12] Ministère de la Santé et des Sports. Plan cancer 2009–2013 [Internet]; 2009
[http://www.sante.gouv.fr/IMG/pdf/Plan_cancer_2009-2013.pdf. Accessed 30/
11/2016].
[13] Institut national du cancer. Détection précoce des cancers de la cavité buccale
[Internet]; 2009 [http://www.e-cancer.fr/Professionnels-de-sante/Depistage-
et-detection-precoce/Detection-precoce-des-cancers-de-la-cavite-buccale/
Modules-de-formation-multimedia. Accessed 30/11/2016].
[14] Pornet C, Delpierre C, Dejardin O, Grosclaude P, Launay L, Guittet L, et al.
Construction of an adaptable European transnational ecological deprivation
index: the French version. J Epidemiol Community Health 2012;66(11):982–9.
[15] Charlson M, Szatrowski TP, Peterson J, Gold J. Validation of a combined
comorbidity index. J Clin Epidemiol 1994;47(11):1245–51.
89
[16] Ligier K, Dejardin O, Launay L, Benoit E, Babin E, Bara S, et al. Health
professionals and the early detection of head and neck cancers: a popula-
tion-based study in a high incidence area. BMC Cancer 2016;16:456.
[17] Adrien J, Bertolus C, Gambotti L, Mallet A, Baujat B. Why are head and neck
squamous cell carcinoma diagnosed so late? Influence of health care dispar-
ities and socioeconomic factors. Oral Oncol 2014;50(2):90–7.
[18] Stefanuto P, Doucet JC, Robertson C. Delays in treatment of oral cancer: a
review of the current literature. Oral Surg Oral Med Oral Pathol Oral Radiol
2014;117(4):424–9.
[19] Reid BC, Warren JL, Rozier G. Comorbidity and early diagnosis of head
and neck cancer in a Medicare population. Am J Prev Med 2004;27(5):
373–8.