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Original Article

Factors influencing delayed referral of oral
cancer patients from family dentists to thecore hospital
Momoka Watanabe ay, Mariko Arakawa ay, Shigeo Ishikawa b*,
Kazuyuki Yusa b, Tomoharu Hemmi b, Naoki Okuyama b,
Satoshi Kasuya b, Nobuyuki Sasahara b, Nagiko Suzuki b,
Manato Sekiguchi b, Kaori Maehara b, Mitsuyoshi Iino bab

Faculty of Medicine, Yamagata University, Yamagata, Japan
Department of Dentistry, Oral and Maxillofacial Plastic and Reconstructive Surgery, Faculty of
Medicine, Yamagata University, Yamagata, Japan

Received 26 April 2023; Final revision received 16 May 2023

Available online - - -KEYWORDS
Family dentists;
Japan;
Oral cancer;
Referral delay;
Risk factors

Abstract Background/purpose: Most oral cancer (OC) cases are identified by family dentists
in Japan. However, a significant number of patients with OC in Japan are referred to core hospitals at advanced stages. Therefore, identifying the factors that contribute to delayed referrals from family dentists to core hospitals is crucial for detecting OC in its earlier stages. The
aim of this retrospective study was to identify the risk factors for referral delays from family
dentists to core hospitals.
Materials and methods: The study included 63 patients with OC who were referred by family
dentists to the Yamagata University Hospital between 2010 and 2022. The clinical parameters
related to referral delays were retrospectively investigated using letters of reference provided
by the family dentists and patient charts. Backward multiple regression analysis was performed to identify the relationships between the length of referral delay and potential risk
factors. Additionally, backward multivariate logistic regression analysis was performed to
examine the independent association between referral delays of >4 weeks and several clinicalparameters.
Results: Multiple regression analysis revealed that misdiagnosis of malignant lesions by family
dentists (P Z 0.047) was significantly associated with longer referral delays. Additionally,
misdiagnosis of malignant lesions by family dentists was also an independent risk factor for
referral delays of >4 weeks (odds ratio, 10.387; P Z 0.006).

* Corresponding author. Department of Dentistry, Oral and Maxillofacial Plastic and Reconstructive Surgery, Faculty of Medicine, Yamagata University, 2-2-2 Iida-Nishi, Yamagata, 990-9585, Japan.
E-mail address: shigeo_ishikawa2011@yahoo.co.jp (S. Ishikawa).
yM. Watanabe and M. Arakawa contributed equally to this work.
https://doi.org/10.1016/j.jds.2023.05.017
1991-7902/ª 2023 Association for Dental Sciences of the Republic of China. Publishing services by Elsevier B.V. This is an open access article under
the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article as: M. Watanabe, M. Arakawa, S. Ishikawa et al., Factors influencing delayed referral of oral cancer patients fromfamily dentists to the core hospital, Journal of Dental Sciences, https://doi.org/10.1016/j.jds.2023.05.017

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M. Watanabe, M. Arakawa, S. Ishikawa et al.
Conclusion: Misdiagnosis of malignant lesions by family dentists was a significant risk factor for
referral delays from family dentists to core hospitals. Our results will motivate family dentists
to improve their ability to diagnose OC.
ª 2023 Association for Dental Sciences of the Republic of China. Publishing services by Elsevier
B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.
org/licenses/by-nc-nd/4.0/).

been performed in other countries,20e22 to our knowledge,
no previous study has surveyed the risk factors for referral
delays in Japan.

Introduction
Oral cancer (OC) occurs in different sites of the oral cavity,
such as the tongue, gingiva, oral floor, buccal mucosa,
palate, and lips. OC occurs commonly worldwide,1e4 and its
incidence has been increasing.5,6 The increasing incidenceof OC is compounded by the low survival rate associatedwith the disease. Despite improvements in the effectiveness of surgery, radiation, and chemotherapy, the survival
rate for OC has not improved significantly.6e8 The survival
rate for advanced-stage OC is extremely low, whereas for
OC diagnosed in the initial stage is relatively higher.3,4,7,8
The low quality of life (QOL) after surgery is another disadvantage.6,9e11 The oral cavity plays important functional
and aesthetic roles in daily activities, such as eating andspeaking and maintaining the constitution of the face,which are necessary for maintaining a high QOL.6,9,10 In
advanced-stage OC, wide local resection leads to oral
dysfunction and aesthetic dissatisfaction.10 Therefore, aswith cancers at other sites, detection of OC at an earlystage is desirable, and referring patients to a core hospitaland beginning treatment as early as possible are
essential.11e14
OC is evaluated by visual examinations.12 Although thedetection of OC is often assumed to be simple, it is not,especially in the initial stage, since initial-stage OC
generally presents with no pain, bleeding, or hypesthesia.15,16 Therefore, most patients with initial-stage OC
do not notice malignant lesions in the oral cavity bythemselves. Furthermore, OC in the initial stage may mimic
benign lesions.17,18 Unfortunately, even general dental
practitioners and family dentists may find it difficult todistinguish early-stage OC from benign lesions.11,12 Most
family dentists in Japan see only a very limited number of
OC cases over the course of their careers. Therefore,
approximately 38.5% of patients with OC in Japan arereferred to core hospitals at advanced stages, such as stage
III or IV.19
Majority of the cases of OC are identified by family
dentists in Japan, who then refer these patients to core
hospitals for the treatment of OC. Therefore, the relevant
factors related to family dentists should be thoroughly
understood to ensure early detection of OC in patients inJapan. Thus, a survey of the risk factors for delayed
referral of patients with OC by family dentists to core
hospitals will facilitate early OC detection by family
dentists.
Therefore, we conducted a retrospective study toidentify the risk factors for referral delays by family dentists. We hypothesized that referral delays are influenced
by family dentists’ diagnostic errors, tumor size, and thesite of occurrence of OC. Although investigations on theeffect of these factors on diagnosis and referral delays have

Materials and methods
Study design and participantsThis study was approved by the Ethics Committee of
Yamagata University School of Medicine (No. 2022-283). Allprocedures involving human participants were conducted inaccordance with the ethical standards of the institutional
and/or national research committee and the 1964 Declaration of Helsinki and its later amendments or comparable
ethical standards.
The present investigation was a retrospective study
conducted using chart data. Consent was obtained throughan online opt-out method, and none of the patients withdrew participation. The study participants included 189
patients with OC recruited from the Department of
Dentistry, Oral and Maxillofacial Surgery, Yamagata University Hospital, between April 2010 and July 2022. Amongthe 189 patients, 94 were excluded, as they were notreferred by family dentists. Furthermore, 32 patients were
excluded because of insufficient information in the referral
letters, such as missing information on the diagnosis by thefamily dentist or the date of the first visit to the family
dentist. Thus, 63 patients with OC were finally included inour statistical analyses.

Measurements
Age, sex, diagnosis by family dentists, cancer site, T-classification, year of medical examination, and the duration of
the consultation were evaluated in relation to referral delays. The duration of consultation was defined as thenumber of days from the day of the patient’s visit to thefamily dentist to the day when they were referred to our
hospital by the family dentist.

Statistical analyses
The ManneWhitney U and chi-squared test were conducted
to evaluate the distribution of characteristics quantitatively and qualitatively, respectively. Backward multiple
regression analysis was performed to investigate the relationship between the length of the referral delay and thepotential risk factors. First, a univariate regression analysis
was performed to identify the potential risk factors forlonger referral delays. Variables with P-values <0.25 in theunivariate analysis were selected as representative variables, and backward multiple regression analysis was2

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Journal of Dental Sciences xxx (xxxx) xxx
Table 1

Characteristics of the participants.
Duration to be referred from the family dentist<4 weeksAge (years)
Sex
Diagnosis in referral
Site of oral cancer
T-classification
Year of medical examination

Male
FemaleTumor
Other than tumor
Gingiva
Other
0-II
III-IV
2010e20162017e2022

P-valuey

4 weeks

Median (min-max)

S.E

Median (min-max)

S.E

73 (23e94)
n

2.0
%

78 (38e90)
n

5.4
%

0.609

29
25
44
10
18
36
40
14
21
33

53.7
46.3
81.5
18.5
33.3
66.7
74.1
25.9
38.9
61.1

4
5
3
6
5
4
4
5
2
7

44.4
55.6
33.3
66.7
55.6
44.4
44.4
55.6
22.2
77.8

0.725
0.006*
0.267
0.114
0.467

y P-value according to Student’s t-test.
* Statistically significant (P < 0.05).
Note: SE, standard error.

performed with the representative variables for longer
referral delays. To examine the independent association
between referral delays of >4 weeks and several clinicalparameters, we also performed backward multivariate logistic regression analysis to estimate the adjusted odds
ratios (ORs) and 95% confidence intervals (CIs). The multivariate logistic regression analysis included representative
variables with P < 0.25 in the univariate logistic analysis.
Statistical significance was set at P < 0.05. All statisticalanalyses were performed using SPSS version 25.0 (IBM,Armonk, NY, USA).

Results
Table 1 presents the distribution of the characteristics ofthe participants divided by the duration of consultation (<4weeks and 4 weeks). The distribution of diagnoses byfamily dentists differed significantly between the twogroups.
Fig. 1 shows the year-wise distribution of 63 patientswith OC. The minimum was zero patients in 2010 and 2011,
and the maximum was nine patients in 2017 and 2019. The
median was six cases of OC.
Table 2 summarizes the results of the univariate andmultiple regression analyses performed to determine theeffects of each parameter on the length of referral delay.
Univariate regression analysis revealed three variables with
P-values <0.25, including misdiagnosis by family dentists,gingival site, and lower T-classifications such as 0, 1, and 2.
Furthermore, multivariate logistic regression analysis withthese three representative factors revealed that misdiagnosis of malignant lesions by family dentists (P Z 0.047,
b Z 0.251) was significantly associated with a longer
referral delay. The adjusted coefficient of determination(R2) for this model was 0.048.
Table 3 also lists the significant variables in the multivariate logistic regression analysis using the variables with

Figure 1
cancer.

Year-wise distribution of 63 patients with oral

P < 0.25 in the univariate analysis. The independent risk
factor for referral delay of >4 weeks was the misdiagnosis
of malignant lesions by family dentists (OR, 10.387; 95% CI,
1.977e54.571; P Z 0.006). Lower T-classifications such as0, 1, and 2 were not significant risk factors (OR, 4.556; 95%
CI, 0.872e23.810; P Z 0.072); however, this variable wasselected in the final logistic model to explain the risk ofreferral delay.

Discussion
In the present study, we surveyed the risk factors fordelayed referral of patients with OC from family dentists tocore hospitals and showed that misdiagnosis of malignant
lesions by family dentists was a significant risk factor for
prolonged referral delays. The present results may give theimpression of being the natural result for dentists.
Furthermore, most dentists may have recognized our3

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M. Watanabe, M. Arakawa, S. Ishikawa et al.
Table 2

Backward multiple regression analysis of the risk factors for referral delay.
Univariate

Multivariate

Variable

B

S.E

ß

t

P-value B

Age (years)
Sex (female vs. male)
Diagnosis in referral (except tumor vs. tumor)
Site of oral cancer (gingiva vs. except gingiva)
T-classification (0-II vs. III, IV)
Year of medical examination(2017e2022 vs. 2010e2016)

0.002
4.87914.4339.248
10.672
5.543

0.220
6.388
7.129
6.552
6.850
6.620

0.001
0.097
0.251
0.178
0.196
0.107

0.010
0.764
2.025
1.411
1.558
0.837

0.992
0.448
0.047*
0.163
0.124
0.406

S.E

ß

t

P-value

14.433 7.129 0.251 2.025 0.047**Statistically significant (P < 0.05).
Note: SE, standard error.
Adjusted for representative variables that were marginally significant in univariate analysis (P < 0.25).

Table 3

Crude and adjusted odds ratios and 95% confidence intervals for the risk for referral delay of more than 4 weeks.

Variable

Crude OR (95% CI)

P-value Adjusted OR (95% CI)

Age (years) (per 1-year increase)
Sex (female vs. male)
Diagnosis in referral (except tumor vs. tumor)
Site of oral cancer (gingiva vs. except gingiva)
T-classification (0-II vs III, IV)
Year of medical examination(2017e2022 vs. 2010e2016)

1.010
1.450
8.800
2.500
3.571
2.227

0.701
0.608
0.006*
0.210
0.085
0.346

(0.960e1.063)(0.351e5.995)(1.874e41.323)(0.597e10.461)(0.839e15.207)(0.422e11.761)

P-value

10.387(1.977e54.571) 0.006*

4.556(0.872e23.810) 0.072*Statistically significant (P < 0.05).
Note: OR, odds ratio. CI, confidence interval.
Adjusted for representative variables that were marginally significant in univariate analysis (P < 0.25).

this study, it remains clinically important, and family dentists should especially consider patients with small lesions.
We hypothesized that the site of cancer in the oral cavity
affects referral delays, and we compared the risk of prolonged referral delays between gingival cancer and cancers
at other sites. Most family dentists in Japan are generalpractitioners; therefore, the majority of their routine cases
involve the treatment of dental caries and periodontitis. In
particular, family dentists frequently treat patients withgingivitis or periodontitis. We hypothesized that the dentists’ familiarity with gingival examinations also makes themaccustomed to seeing severe gingival inflammation. Since
gingival inflammation and malignancy are often similar inappearance,17,18,25 family dentists may have a high thresholdfor the diagnosis of gingival malignancy, and they may diagnose a malignant gingival lesion as gingival inflammation,
leading to prolonged referral delays. However, in the present
study, the gingival site of OC was not a significant risk factor
for referral delays. If a specific OC site is confirmed as a risk
factor for referral delays, it can be used as a cue for family
dentists to focus their examinations. Further studies are
required to clarify this point.
The possibility that several family dentists do not havesufficient knowledge of OC has been pointed out in a previous study.29 One reason for this may be the nature ofuniversity education in dentistry. Ozdemir-Ozenen reported
that dental university students in Istanbul, Turkey, hadinsufficient knowledge regarding some of the main concepts of OC risk factors, and they lacked confidence inresults clinically and intuitively, as several reports havealready identified insufficient knowledge of OC among
general dental practitioners.23,24 However, to our knowledge, no scientific study has comprehensively surveyed therisk factors for referral delays in Japan, and our study
represents the first attempt to confirm significant risk factors for referral delays in Japan. These factors highlight therelevance of our findings.
In the present study, a low T-classification was not a
statistically significant risk factor for prolonged referral
delays; however, it showed a slight significance in the final
logistic models (P Z 0.072). This result will also be clinically and intuitively accepted by most dentists. Larger lesions, which indicate higher T-classifications, are very easy
to detect by visualization assessments. In general, OC witha higher T-classification, especially more than T3, shows
several notable clinical features, such as remarkable ulceration and lumps.16 Thus, even if the family dentist has
no experience in diagnosing OC clinically, they will be able
to recognize the lesion and refer the patient to a core
hospital. In contrast, smaller OC lesions may be difficult torecognize for family dentists with no specialization in oral
surgery, as these smaller lesions generally mimic thecharacteristics of benign lesions.17,18,25,26 Moreover, patients with smaller OC lesions generally do not experience
any symptoms,16 and patients with OC may have little
knowledge of the disease.27,28 Thus, patients with smaller
OC lesions may not present with any complaints. Thus,
although T-classification was not statistically significant in4

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Journal of Dental Sciences xxx (xxxx) xxx
examining their patients.30 They also highlighted the needto change the curriculum in dental universities.30 Similar
surveys have been performed worldwide and suggestions
provided for improving the OC educational curriculum fordental students.31e35 These changes in undergraduate
dental education are essential for improving OC diagnosis
skills among family dentists and shortening referral delays.
Our study has a few limitations. The first limitation isrelated to the generalizability of the findings due to missing
data. The number of patients with original OC was 189,
among whom 95 were referred by family dentists. However,among these 95 patients, 32 were excluded, as their lettersof referral did not include information regarding the day of
the first visit to the family dentist and/or the diagnosis by thefamily dentist. In future studies, this information should becollected through direct interviews with the family dentist
instead of relying on letters of reference. The second limitation was that the adjusted coefficient of determination(R2) in this model was low. Only a limited number of confounding factors were adjusted for in our model; thus, otherrelevant confounding factors may not have been adjusted forin our model. For example, the specialty of the family dentist
affects the duration of the consultation. Oral surgeons havehigh accuracy in discriminating OC from other lesions. Thus,
if the family dentist has an extensive background in oral
surgery training, the referral delay may be minimized. Thus,
a thorough assessment of additional and appropriate confounding factors will be required to improve the study designin future investigations. The third limitation is that our study
only surveyed the referral delay from family dentists, which
is a part of professional delays in diagnosis. Diagnostic delay
in OC is typically defined as the interval between symptom
onset and histological diagnosis36 and consists of twoparts20,37: patient delays and professional delays. Patientdelay refers to the interval between the day patients experience some symptoms of OC to the day they visit any medical
facility. Professional delay refers to the time from the firstpresentation to the health practitioner to the histologicaldiagnosis. Our study primarily investigated professional
delay. As patient delay has been reported to have a greater
influence on OC than professional delays,20,36,37 futurestudies should aim to comprehensively evaluate both aspects
while surveying the risk factors for diagnostic delays inJapan.
In summary, we showed that misdiagnosis of malignant
lesions by family dentists was a significant risk factor fordelayed referrals to core hospitals. Family dentists should
unequivocally remain the first line of screening for OC. Our
results will motivate family dentists to improve their ability
to diagnose OC.

editage.com) for English language editing. This research did
not receive any specific grant from funding agencies in the
public, commercial, or not-for-profit sectors.

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Declaration of competing interest
The authors have no conflicts of interest relevant to thisarticle.

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