RESEARCH REPORTS
Clinical
W. Pitiphat1,2,3, S.R. Diehl4, G. Laskaris5, V.
Cartsos1, C.W. Douglass1,2, and A.I. Zavras1*
1Department of Oral Health Policy & Epidemiology,
Harvard School of Dental Medicine, 188 Longwood Ave.,
Boston, MA 02115, USA; 2Department of Epidemiology,
Harvard School of Public Health, Boston, MA 02115, USA;
3Department of Community Dentistry, Faculty of Dentistry,
Khon Kaen University, Khon Kaen 40002, Thailand;
4Craniofacial Epidemiology and Genetics Branch, National
Institute of Dental and Craniofacial Research, Bethesda,
MD 20892-6401, USA; and 5Oral Medicine Department, A.
Sygros Hospital, University of Athens Medical School, 37
Ipsiladou Street, Athens 10676, Greece; *corresponding
author, zavras@hms.harvard.edu
J Dent Res 81(3):192-197, 2002
ABSTRACT
Early detection and treatment improve the
prognosis for oral cancer. Delays from the onset of
symptoms to clinical diagnosis are common. Our
aim is to identify factors associated with this delay.
Between 1995 and 1998, we interviewed 105
consecutive patients with histologically confirmed
oral cancer in Greece. If 21 or more days elapsed
from the time the patient noticed major symptoms
to a definitive diagnosis, we called it a delay (52%
of cases). We used logistic and linear regression to
estimate odds ratios of delayed diagnosis and to
identify correlates of length of delay, respectively.
Former smokers had a 4.3 times greater risk of
delayed diagnosis compared with current smokers
(95% confidence interval: 1.1-17.1). The length of
delay was greater among single patients, non-
smokers, or those with stage IV tumors. Clinicians
should be advised that delay in the diagnosis of
oral cancer occurs frequently, even in individuals
who do not smoke heavily.
KEY WORDS: diagnosis, delay, oral cavity, mouth
neoplasms.
Received April 27, 2001; Last revision November 16, 2001;
Accepted January 16, 2002
192
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International and American Associations for Dental Research
Factors Associated
with Delay in the
Diagnosis of Oral Cancer
INTRODUCTION
O ral cancer has one of the lowest five-year survival rates among the major
types of cancer, including breast, skin, testis, prostate, uterus, and
urinary bladder cancers (Pisani et al., 1999), with survival rates often of 50%
or less (Ries et al., 2000). Early diagnosis is crucial to an improved survival
rate. If lesions are detected when they are small, localized, and treated
expeditiously, survival rates of 70 to 90% can be achieved (Silverman, 1988).
The five-year survival rate for persons with localized lesions is four times
greater than that for those with distant metastases (Ries et al., 2000).
Although oral cancer occurs in a part of the body that is readily accessible for
early detection, most lesions are not diagnosed until they have reached advanced
stages. Based on the Surveillance, Epidemiology, and End Results (SEER) data,
at the time of diagnosis of oral cancer, 36% of persons had localized disease, 44%
had regional disease, and 9% had distant disease (Ries et al., 2000).
Previous studies in several populations have shown that there is often a
substantial delay in the diagnosis of oral cancer (Dimitroulis et al., 1992;
Wildt et al., 1995; Hollows et al., 2000). For earlier diagnosis to be
promoted, it is important that the factors predisposing to diagnostic delays
be identified. We therefore examined the extent and determinants of delay in
the diagnosis of oral cancer in the Greek population.
MATERIALS & METHODS
Study Participants and Data Collection
We evaluated factors associated with diagnostic delay among the oral cancer
cases in a hospital-based case-control study in Greece (Zavras et al., 2001). The
study was conducted in 3 major teaching hospitals in Athens, between
November, 1995, and January, 1998. Patients were adults aged 26 to 91 years,
with no prior history of oral cancerC, who were diagnosed with
histopathologically confirmed squamous cell oral or pharyngeal cancer (ICD9
141, 143-145, 148-149). Informed consent was obtained from all patients who
participated in the study. The protocol was reviewed and approved by
Institutional Review Boards of both the Harvard School of Public Health and the
National Institute of Dental and Craniofacial Research (NIDCR/NIH).
Patients were interviewed in the hospital by a trained interviewer using a
structured, pre-tested, questionnaire. Risk factor data included demographic and
socio-economic characteristics, information on tobacco use, alcohol drinking,
family history of cancer, intra-oral status, and weight change. Tumor size and TNM
stage at time of diagnosis were also assessed. We recorded the time interval from
the self-reported date when oral cancer signs and/or symptoms were first noted by
the cases to the date of definitive diagnosis. Some of the most common symptoms
reported by cases included prolonged hemorrhage, pain, existence of a
tumor/nodule, and difficulty in swallowing. A subject was defined as being delayed
J Dent Res 81(3) 2002 Oral Cancer Delay of Diagnosis
if 21 or more days had elapsed between first notice of signs or
symptoms by the subject and the definitive oral cancer diagnosis.
This interval of 3 wks allows for a seven- to 10-day follow-up of a
symptom, a second visit and a biopsy, as well as the time required for
a histopathologist to report the results back to the dentist/physician.
For those subjects who were coded as being delayed, the length of
delay was defined as the number of days beyond the 20th day after
initial symptoms were self-recognized to the date of the definitive
oral cancer diagnosis. For example, if a subject reported that the
interval between first notice of symptoms and definite diagnosis was
90 days, then his/her length of delay was 90 – 20 = 70 days.
Statistical Analysis
We first analyzed the data by comparing the distributions of study
variables between delay and non-delay groups. We evaluated the
statistical significance of differences between the two groups (time
to diagnosis and other continuous variables) using the Wilcoxon
rank-sum test. Odds ratios (OR) and 95% confidence intervals (CI)
were estimated by logistic regression. We utilized multiple linear
regression to identify factors associated with the length of delay
among those subjects who experienced delay of > 21 days. The
following variables were considered: gender, age, education (no
formal education, 1-6 yrs, 7-12 yrs, > 12 yrs of schooling), marital
status (single, married, widowed, separated), employment status
(having being unemployed or not), history of liver cirrhosis (yes,
no), history of sexually transmitted disease (yes, no), family
history of cancer (yes, no), alcohol drinking (never or less than 1
glass/wk, 1-28 glasses/wk, 29-42 glasses/wk, > 42 glasses/wk),
number of missing teeth, weight change, tumor size, and stage of
tumor (advanced = TNM stage IV; earlier = TNM stage I, II, III).
Cigarette smoking was analyzed both as discrete categories (non-
smoker, former smoker, current smoker) and as continuous
exposure (pack yrs). All statistical tests were two-tailed.
RESULTS
During the study period, 105 respondents provided complete
information on the variables of interest. The ratio of males to
females was 1.6:1. Self-reported time to diagnosis varied from 0
to 780 days, with a mean of 80.6 days (SD 157.9) and a median of
30 days. Fifty-five patients exhibited a delay of 21 days or more
(52.4%). Of these patients with a delay in diagnosis, 21 (38.2%)
were diagnosed more than 14 wks after their first symptoms, and
11 (20.0%) more than 30 wks after first symptoms (Fig.).
Most patients were married and employed, and had no
history of liver cirrhosis or sexually transmitted disease. More
than 60% of the cases were not diagnosed until they reached
TNM stage II or beyond. Delay and non-delay groups were
similar in most characteristics (Table 1). There was no
significant difference in the risk of a diagnostic delay between
former smokers and non-smokers, and between current
smokers and non-smokers. The risk was significantly higher
among former smokers than among current smokers (OR, 4.3;
95%CI, 1.1-17.1). No other characteristics were associated with
delay status at significance level of 0.05.
The univariate linear regression analyses performed for the
identification of factors related to the length of delay (among
those cases with 21 or more days’ delay in diagnosis) are
presented in Table 2. Length of delay was significantly longer
in unmarried than in ever-married patients, and in non-smokers
than in ever-smokers. Delay time was marginally associated
with gender and advanced stage of tumor. Weight loss was
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193
Figure. Time to diagnosis for 105 oral and pharyngeal cancer cases
in Greece.
significantly and positively related to the length of delay (p <
0.01), but only in the univariate analyses.
In the multivariate linear regression analyses (Table 3), the
length of delay in diagnosis was significantly associated with
marital status, tobacco use, and advanced stage of tumor. The
diagnosis was delayed approximately 239 days for patients
with TNM stage IV as compared with those with earlier stages
of disease. Past and current smokers were diagnosed on an
average of 133 and 131 days earlier than non-smokers,
respectively. The longest diagnostic delay was associated with
being unmarried, since these subjects experienced delays
estimated to be 170, 383, and 248 days longer than patients
who were married, widowed, and separated, respectively.
DISCUSSION
Fifty-two percent of Greek patients with oral cancer had a
delay in diagnosis of more than 3 wks. The time from initial
symptoms to definitive diagnosis ranged between 0 and 780
days, with a median of 30 days. A study in The Netherlands
reported similar findings (median time of 46 days, range 14
days to 2 yrs) (Jovanovic et al., 1992). A median time to
diagnosis of 3 mos was observed in Canada (Elwood and
Gallagher, 1985) and Italy (Mashberg et al., 1989), compared
with 4 mos in Finland (Söderholm, 1990), Denmark (Wildt et
al., 1995), and Israel (Gorsky and Dayan, 1995). Although our
results are more favorable compared with those of other
populations, the proportion of patients with delay was still
considerably high.
A previous study showed no association between marital
status and oral cancer delay in diagnosis (Elwood and
Gallagher, 1985). In our study, unmarried patients
experienced longer delay than ever-married subjects. Being
unmarried has been reported as associated with less favorable
life-styles and unhealthy behaviors. Unmarried persons may
be less likely to have dental care coverage (Manski, 1995)
and less likely to utilize dental services (Osterberg et al.,
1998). Patients with newly diagnosed and recurrent cancer
who are married appear to experience higher levels of hope,
as assessed by the Herth Hope Scale (Ballard et al., 1997).
Two large longitudinal studies conducted in the US (Johnson
et al., 2000) and the UK (Cheung, 2000) showed that
unmarried persons had an elevated risk of death compared
with married persons.
194 Pitiphat et al. J Dent Res 81(3) 2002

Table 1. Study Characteristics of the Patients According to Status of Delay in the Diagnosis of Oral Cancers

Number (%)
Characteristics Delay (n = 55) Non-delay (n = 50) p-value Odds Ratio (95% CI)

Time to diagnosis in days (mean ± SD) 152.8 ± 191.9 1.0 ± 4.0 < 0.001 Not applicable
(median) 90 0
(range) 25-780 0-20
Age (yrs) (mean ± SD) 64.6 ± 14.0 62.3 ± 15.1 0.65 1.0 (1.0-1.0)a
(range) 26–91 29–87
Gender
Males 33 (60.0) 32 (64.0) 1.0 (Referent)
Females 22 (40.0) 18 (36.0) 0.67 1.2 (0.5-2.6)
Marital status
Single 7 (12.7) 7 (14.00) 1.0 (Referent)
Married 34 (61.8) 32 (64.0) 0.92 1.1 (0.3-3.4)
Widowed 5 (9.1) 5 (10.0) 1.00 1.0 (0.2-5.1)
Separated 9 (16.4) 6 (12.0) 0.59 1.5 (0.3-6.5)
Education
Illiterate 4 (7.3) 9 (18.0) 1.0 (Referent)
1-6 yrs of school 27 (49.1) 19 (38.0) 0.08 3.2 (0.9-11.9)
7-12 yrs of school 17 (30.9) 18 (36.0) 0.27 2.1 (0.6-8.2)
> 12 yrs of school 7 (12.7) 4 ( 8.0) 0.11 3.9 (0.7-21.6)
History of unemployment
No 42 (76.4) 43 (86.0) 1.0 (Referent)
Yes 13 (23.6) 7 (14.0) 0.21 1.9 (0.7-5.2)
History of sexually transmitted disease
No 49 (89.1) 49 (98.0) 1.0 (Referent)
Yes 6 (10.9) 1 ( 2.0) 0.10 6.0 (0.7-51.7)
History of liver cirrhosis
No 52 (94.6) 49 (98.0) 1.0 (Referent)
Yes 3 (5.5) 1 (2.0) 0.38 2.8 (0.3-28.1)
Family history of cancer
No 33 (60.0) 35 (70.0) 1.0 (Referent)
Yes 22 (40.0) 15 (30.0) 0.29 1.6 (0.7-3.5)
Tobacco use
Non-smoker 20 (36.4) 19 (38.0) 1.0 (Referent)
Former smoker 11 (20.0) 3 (6.0) 0.09 3.5 (0.8-14.4)
Current smoker 24 (43.6) 28 (56.0) 0.63 0.8 (0.4-1.9)
Lifetime use (packyears)
Former smoker (mean ± SD) 52.0 ± 45.1 63.3 ± 51.3 1.0 (1.0-1.0)a
(range) 0.2-138.0 20.0-120.0 0.76
Current smoker (mean ± SD) 48.4 ± 27.3 50.6 ± 30.5 1.0 (1.0-1.0)a
(range) 1.5–93.0 5.7–100.0 0.81
Alcohol use
Never 17 (30.9) 18 (36.0) 1.0 (Referent)
1-28 glasses/wk 26 (47.3) 21 (42.0) 0.55 1.3 (0.5-3.2)
29-42 glasses/wk 5 (9.1) 5 (10.0) 0.94 1.1 (0.3-4.3)
> 42 glasses/wk 7 (12.7) 6 (12.0) 0.75 1.2 (0.3-4.4)
Number of unreplaced teeth (mean ± SD) 5.8 ± 9.4 3.9 ± 8.2 0.07 1.0 (1.0-1.1)a
(range) 0–32 0–32
Weight loss (kg) (mean ± SD) 1.7 ± 7.7 2.2 ± 4.7 0.23 1.0 (0.9-1.1)a
(range) -14-45 -2-20
Tumor size (mm) (mean ± SD) 24.7 ± 14.7 24.8 ± 14.5 0.91 1.0 (1.0-1.0)a
(range) 0-60 0-55
TNM staging
I 23 (41.8) 17 (34.0) 1.0 (Referent)
II 15 (27.3) 12 (24.0) 0.64 1.3 (0.5-3.2)
III 9 (16.4) 8 (16.0) 0.83 1.1 (0.4-3.4)
IV 6 (10.9) 5 (10.0) 0.79 1.2 (0.3-4.4)
Unknown 2 (3.6) 8 (16.0)

a Per one unit increase.

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J Dent Res 81(3) 2002 Oral Cancer Delay of Diagnosis 195

Table 2. Simple Linear Regression Analyses of the Association between the Total Delay Time to Diagnosis and Patient's Characteristics (n = 55)

Characteristics Intercept Coefficient Estimate p-value R2

Female gender 96.2 ( 32.8)a 91.7 ( 51.8) 0.08 0.0559

Age 183.5 (123.7) -0.8 ( 1.9) 0.68 0.0033
Marital status 297.1 ( 69.0) 0.1461
Married -163.7 ( 75.7) 0.04
Widowed -269.1 (106.8) 0.01
Separated -236.1 ( 91.9) 0.01
Education 25.0 ± 96.2 0.0493
1-6 yrs of school 103.5 (103.1) 0.32
7-12 yrs of school 156.4 (107.0) 0.15
> 12 yrs of school 68.3 (120.7) 0.57
Having history of unemployment 126.4 (29.8) 27.4 ( 61.4) 0.66 0.0038
Having history of liver cirrhosis 139.3 (26.6) -119.3 (113.8) 0.30 0.0203
Having history of sexually transmitted disease 128.3 (27.6) 41.7 ( 83.6) 0.62 0.0047
Having family history of cancer 160.2 (33.2) - 68.4 ( 52.5) 0.20 0.0311
Tobacco use 228.4 (40.4) 0.1447
Former smoker -157.5 ( 67.9) 0.02
Current smoker -146.7 ( 54.7) < 0.01
Lifetime use (packyrs) 177.0 (33.8) -1.4 ( 0.7) 0.05 0.0679
Alcohol use (glasses per wk) 121.9 (47.1) 0.0338
1-28 42.4 ( 60.5) 0.49
29-42 -15.9 ( 98.7) 0.87
> 42 -60.5 ( 87.2) 0.49
Number of unreplaced teeth 119.3 (32.6) 3.0 ( 3.0) 0.32 0.0203
Weight loss in kg 120.0 (25.4) 8.9 ( 3.2) < 0.01 0.1270
Advanced stage of tumor
(TNM stage IV) 119.1 (27.8) 150.9 ( 82.52) 0.07 0.0615
Tumor size in mm 121.9 (49.3) 0.02 ( 1.7) 0.99 < 0.0001

a Numbers in parentheses are standard errors.

Our finding of an absence of significant Table 3. Multiple Linear Regression Analysis to Identify Predictors of Delay Days in
association between age and diagnostic delay is Diagnosis
consistent with findings from other studies in oral
cancer patients (Elwood and Gallagher, 1985; Characteristics Parameter Estimate Standard Error p-valuea
Guggenheimer et al., 1989; Jovanovic et al., 1992)
and in head and neck cancer patients in general Intercept 372.5 66.3 < 0.001
(Amir et al., 1999). One study showed a Marital status
significant but weak correlation between female Married -169.5 67.9 0.02
gender (r = 0.26) and older age (r = 0.19) with Widowed -382.6 107.0 < 0.001
professional delay (interval between first visit until Separated -247.8 82.4 < 0.01
definitive diagnosis), but not with patient delay Tobacco use
(interval between onset of symptoms to first visit Former smoker -132.5 64.2 0.04
to a physician) (Wildt et al., 1995). A recent study Current smoker -131.1 50.7 0.01
of tongue cancer found that fatal delays too often Advanced stage of tumor
occurred when the initial professional evaluation (TNM stage IV) 239.4 82.0 0.01
did not lead to a follow-up referral for further a Adjusted R2 = 0.3324.
examination (Kantola et al., 2001). In Thailand,
prolonged patient delay was associated with the
use of traditional herbal medicine (Kerdpon and
Sriplung, 2001), highlighting how local social and cultural factors measures for socio-economic status, such as education level and
need to be taken into consideration for different populations. unemployment, were found not to affect the timing to diagnosis.
We found no association between gender and education and Since it is known that socio-economic status (SES) affects the five-
delay in diagnosis. Similar results have been reported by various year survival rate, as is the case with US blacks as compared with
workers (Guggenheimer et al., 1989; Jovanovic et al., 1992; Amir whites, residual confounding cannot be ruled out. Our study
et al., 1999); one study observed a longer time to diagnosis in focused on patients being diagnosed at public hospitals of the
females than in males, but these results were only marginally National Healthcare System. A future study is needed to assess
significant (p = 0.05) (Elwood and Gallagher, 1985). Surrogate those who are diagnosed or treated at private hospitals.

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International and American Associations for Dental Research

196
Our findings suggest a strong association between history
of sexually transmitted disease and delay in diagnosis. History
of a sexually transmitted disease may be associated with
personal behaviors that were not assessed in the present work,
such as low healthcare services utilization. For the exact nature
of this interesting association to be assessed, more studies are
needed. These studies need to control for residual confounding,
in addition to having adequate statistical power.
Theoretically, one would expect that longer delay would be
associated with more advanced stages of disease at diagnosis.
We confirmed this theory only for TNM stage IV. In one study,
patients with TI cancers had a shorter delay than patients with
larger lesions, but patients with TII, TIII, and TIV cancers were
similar in length of delay (Mashberg et al., 1989). Other studies
indicated no association of tumor staging with overall delay
(Guggenheimer et al., 1989; Söderholm, 1990; Jovanovic et al.,
1992; Kowalski et al., 1994), patient delay (Kowalski et al.,
1994; Wildt et al., 1995; Hollows et al., 2000), or professional
delay (Wildt et al., 1995; Hollows et al., 2000). Apart from
possible population differences, the discrepancies in these results
may be explained in several ways. First, we performed a multiple
linear regression using length of delay as the dependent variable,
while most of the above-mentioned studies performed bivariate
categorical analyses, comparing the distribution of tumor staging
among categories of number of wks or mos of delay. Classifying
length of delay into categories may be subject to
misclassification, leading to null results. Second, we focused our
analyses on the subgroup of patients who had delay in diagnosis,
because our main research question was to identify factors that
influence the length of delay. To determine the robustness of our
method, we also performed the analyses on all our study patients
(data not shown), and found that the results were similar,
although the association between Stage IV and length of delay
became only marginally significant (p = 0.06).
The absence of a significant association between delay in
diagnosis and alcohol use is in agreement with the literature
(Elwood and Gallagher, 1985; Guggenheimer et al., 1989;
Hollows et al., 2000). Previous studies also found no association
between delay and smoking habit (Elwood and Gallagher, 1985;
Hollows et al., 2000). We found a significant relationship of delay
with smoking history, but not with the quantity consumed, with
former smokers being more likely to have delay in diagnosis as
compared with current smokers. Among patients with delay, non-
smokers had a longer delay than both former and current smokers.
It is possible that being a non-smoker may generate a false feeling
of security for both the patient and the physician. Another possible
explanation is that smokers might seek professional attention more
often than non-smokers (Rodriguez Artalejo et al., 2000), due to a
variety of chronic medical, dental, and smoking-related conditions,
thereby resulting in an earlier diagnosis of oral cancer.
Assessment of the time to diagnosis depended on patients’
recollection of their first symptoms, and thus, this is a limitation
of our study. It is possible that subjects did not correctly recall the
onset of symptoms, especially when the delayed period was very
prolonged. Although there may be measurement error in
estimates of the length of delay, we doubt that there is substantial
misclassification of our subjects as being delayed or not, since the
median number of days of delay differ so dramatically between
these groups (90 vs. 0 days). Another limitation is our inability to
distinguish if the delay is due to the patient or the clinician, and
thus, to infer the true causes of observed delays.
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International and American Associations for Dental Research
Pitiphat et al. J Dent Res 81(3) 2002
Our study confirms previous international reports regarding
the magnitude of the problem and sets the stage for additional
investigations of the reasons for diagnostic delays and the
potential for the development of effective strategies for reducing
this serious problem. Such strategies should consider the long
delays observed in subjects who are not exposed to high-risk
behaviors such as smoking and heavy drinking. The fact that
delay was associated with the stage with the highest morbidity
and mortality, Stage IV oral cancer, should alert clinicians and
the public about the value of early detection. Rigorous
educational programs targeting both the general public and
health professionals (Yellowitz et al., 2000), supplemented by
innovative diagnostic strategies, such as the use of tolonium
chloride for high-risk groups (Kerawala et al., 2000) or the use
of brush biopsy cytological detection of abnormalities (Sciubba,
1999), promise to lower the burden of oral cancer.
ACKNOWLEDGMENTS
The authors acknowledge the support of Drs. J. Segas, P.
Nomikos, D. Lefantzis, G. Dokianakis, and P. Thomas. Special
thanks to A. Pantelidakis for serving as interviewer, to Dr.
Mohammad Khoshnevisan, Dr. Kaumudi Joshipura, and
Renukha Bahadursingh for review and editorial assistance in
the preparation of the manuscript. This study was partially
supported by NIDCR/NIH K23DE00420 grant and by NIDR
contracts MD 626829 and 726655.
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