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J Canc Educ

DOI 10.1007/s13187-015-0823-2

Factors Influencing Early Detection of Oral Cancer by Primary


Health-Care Professionals
Y. Hassona 1 & C. Scully 2 & A. Shahin 1 & W. Maayta 1 & F. Sawair 1

# American Association for Cancer Education 2015

Abstract The purposes of this study are to determine early early diagnosis of oral cancer and oral mucosal lesions are
detection practices performed by primary healthcare profes- needed for primary health-care professionals.
sionals, to compare medical and dental sub-groups, and to
identify factors that influence the ability of medical and dental Keywords Oral cancer . Early diagnosis . Diagnostic ability .
practitioners to recognize precancerous changes and clinical Knowledge . Practice
signs of oral cancer. A 28-item survey instrument was used to
interview a total of 330 Jordanian primary health-care profes-
sionals (165 dental and 165 medical). An oral cancer knowl- Introduction
edge scale (0 to 31) was generated from correct responses on
oral cancer general knowledge. An early detection practice Oral cancer is a significant world health problem. It is the sixth
scale (0 to 24) was generated from the reported usage and most common cause of cancer-related deaths [1]. The known
frequency of procedures in oral cancer examination. Also, a etiology of oral cancer is primarily linked to tobacco use,
diagnostic ability scale (0 to 100) was generated from correct alcohol consumption, betel use, and combinations of these
selections of suspicious oral lesions. Only 17.8 % of the par- habits. Human papillomavirus (HPV) infection is implicated
ticipants reported that they routinely performed oral cancer mainly in oropharyngeal cancer, and ultraviolet light is the
screening in practices. Their oral cancer knowledge scores main factor in lip cancer. Many other factors are possibly
ranged from 3 to 31 with a mean of 15.6. The early detection implicated in mouth, lip, and oropharyngeal cancers, includ-
practice scores ranged from 2 to 21 with a mean of 11.6. A ing immunosuppression, familial and genetic factors, diet, and
significant positive correlation was found between knowledge socioeconomic status [2]. Some cancers are preceded by oral
scores and early detection practice scores (r=0.22; p<0.001). potentially malignant disorders (OPMD) such as
The diagnostic ability scores ranged from 11.5 to 96 with a erythroplakia, leukoplakia, or actinic cheilitis.
mean of 43.6. The diagnostic ability score was significantly The oral cavity is easily accessible and can be examined
correlated with knowledge scores (r=0.39; p<0.001), but not with little discomfort. It is unfortunate however, that most oral
with early detection practice scores (r=0.01; p=0.92). Few cancers, even in developed countries, are detected at late
significant differences were found between medical and dental stages [2]. The evidence suggests that earlier diagnosis of oral
primary care professionals. Continuous education courses on cancer leads to less complex treatment and improved progno-
sis and quality of life [3]. Usually, patients with oral cancer are
first seen by primary health-care professionals (HCPs), mainly
Electronic supplementary material The online version of this article
(doi:10.1007/s13187-015-0823-2) contains supplementary material, medical and dental. Emphasis therefore has been placed on
which is available to authorized users. opportunistic screening of the oral mucosa by HCPs as a pro-
active preventative measure which may lead to reduced mor-
* Y. Hassona bidity and mortality from oral cancer [4].
yazan@ju.edu.jo Several studies have been conducted in different parts of
the world to assess the knowledge, opinions, and practices of
1
Department of Oral and Maxillofacial Surgery, Oral Medicine, and HCPs regarding oral cancer and in the main, revealed an in-
Periodontology, Faculty of Dentistry, The University of Jordan, PO adequate level of knowledge about oral cancer including lack
Box 11942, Amman, Jordan of knowledge about risk factors and proper examination tech-
2
University College London, London, UK niques [4–17]. Most of these studies have used self-reported
J Canc Educ

surveys that paid little attention to details of specific proce- terminology, and Arabic translation of medical terms was
dures that health-care workers perform as part of their practice available upon request. The interview questionnaire elicited
related to oral cancer detection [15]. Many medical students information about demographics, knowledge of oral cancer,
and doctors appear unaware of some risk factors (e.g., alcohol) early detection practices, and attendance of continuing profes-
as a risk factor for oral cancer or that erythroplakia and sional development courses on oral cancer. The knowledge
erythroleukoplakia are early signs of oral cancer [16]. One section included questions about risk factors and epidemiolo-
study found that GDPs were able to list a mean of 2.75 chang- gy of oral cancer, oral lesions/conditions that might transform
es associated with oral cancer, compared to that of GMPs (a to cancer, clinical signs and symptoms of oral cancer, and
mean of 1.75 changes identified); while most clinicians sur- techniques that might help in early detection of oral cancer.
veyed identified mouth ulceration (70 % GMPs, 80 % GDPs), Responses to knowledge questions were assessed as cor-
few reported speckled leukoplakia or erythroleukoplakia [17]. rect or incorrect, and Bknowledge scores^ were calculated for
In addition, none of these studies have directly examined the each respondent. Score 31 indicated that the participant an-
ability of primary HCPs to recognize precancerous changes or swered all the factual questions about oral cancer correctly,
clinical signs suggestive of early cancer. and score zero indicated that the participant failed to answer
The purposes of the present study therefore were to deter- any question correctly or answered BI do not know^ for all
mine the declared thoroughness of examination and early de- questions. To assess the components of early detection prac-
tection practices performed by primary HCPs, to compare the tices performed by participants, a series of questions probed
performances of dental and medical primary care practi- specific examination procedures and the frequency of perfor-
tioners, and to identify factors that influence their ability to mance. For each procedure, points were assigned as follows:
recognize precancerous changes and clinical signs of oral always=3, sometimes=2, only upon complaint/rarely = 1, and
cancer. never=0. BEarly detection practices scores^ were calculated
for each respondent by summing the scores across each pro-
cedure. Questions used to generate the Bknowledge scores^
Materials and Methods and Bearly detection practices scores^ are available as supple-
mentary material.
The University of Jordan, Amman, Faculty of Dentistry Re- In addition, the interviewers showed participants a collec-
search and Ethics Committee (FDREC) reviewed and ap- tion of clinical images that represented a wide spectrum of oral
proved the study which was conducted in full accordance with mucosal diseases including benign, potentially malignant
the World Medical Association Declaration of Helsinki. (precancerous), and malignant conditions. A total of 52 clin-
A total of 380 primary HCPs practicing in Amman (190 ical images were shown, and participants were asked to
dental practitioners and 190 medical practitioners) were ran- choose images that they would consider Bsuspicious for
domly selected by choosing the first, middle, and last names malignancy^. Clinical images used were from the authors’
from each page in the registries of the Jordanian Medical own collection, which could not have been previously viewed
Association and the Jordanian Dental Association to partici- by participants, and were validated for adequacy and clarity
pate in the study. Sample size was calculated using nQuery by an independent group of specialists in oral medicine. Of the
Advisor Software with oversampling to account for possible 52 clinical images, 26 represented OPMDs or early cancer and
withdrawals. Participants’ offices were contacted by phone to judged by the specialists group to be Bsuspicious for
arrange for appointments. From this 380, 50 practitioners (25 malignancy^ according to the clinical appearance. The rest of
dentists and 25 medical practitioners) did not participate be- the clinical images represented common benign oral conditions.
cause they were either not interested or were busy at the sur- The clinical images are available as supplementary material.
vey time. The final sample thus consisted of 330 primary The ability of participants to recognize Bsuspicious
HCPs (165 medical practitioners and 165 dental practitioners) lesions^ was measured in terms of sensitivity according to
of mixed genders and various ages and time from qualification the following formula: ability to recognize a suspicious lesion
(see BResults^). We assessed the representativeness of the = (X/26)×100 % where X represents the number of images
sample by comparing the characteristics of those who were correctly identified by the participant as Bsuspicious for
selected with the national health workforce profiles [18]. malignancy^ and 26 represents the actual number of clinical
Two coauthors (AS and WM together) simultaneously images that are truly suspicious for malignancy [19].
interviewed all participants to avoid any bias that could result Statistical analysis was performed using SPSS for Win-
from variations in conducting the interview. Both coauthors dows release 16.0 (SPSS Inc., Chicago, IL, USA). Descriptive
were trained to perform a professional interview. The purpose statistics were generated. Student’s t test and Pearson’s Corre-
of the study was explained, and participants were reassured lations test (r) were used to examine differences and correla-
that no personal identifying information would be disclosed. tions between groups. Results were considered significant if
The interview was conducted using English for medical p values were less than 0.05.
J Canc Educ

Results When asked about the possible clinical presentations of


oral cancer, participants were more knowledgeable of the later
Of the 330 respondents, 233 (70.6 %) were males and 97 signs/symptoms of oral cancer such as enlarged lymph nodes
(29.4 %) were females. Half of the participants (n=165) were (71.8 %), ulcerated lump (67.6 %), limited tongue mobility/
general medical practitioners, and the other half (n=165) were dysphagia (67.3 %), and pain (65.2 %). Fewer participants
practicing dentists. The years of clinical practice of partici- however knew early presentations of oral cancer such as white
pants ranged from one to fifty two (median 12.5 years±11.2). patch (46.4 %), red patch (42.4 %), and delayed healing of
Almost half of the participants (49.4 %) reported that they extraction sites (43 %).
had seen at least one patient with oral cancer or OPMD—either The majority of participants knew that scalpel biopsy is still
during their practice or training. Almost all participants (96.7 %) the main diagnostic aid in oral cancer and OPMDs. Fewer
were able to identify tobacco as a main risk factor for oral cancer. participants however were aware of the existence of other
Nearly half of the participants correctly identified alcohol diagnostic techniques such as exfoliative cytology (51.5 %),
(57.3 %), chewing habits (53.9 %), and human papillomavirus brush biopsy (35.8 %), fluorescent lights (27 %), and toluidine
(43.3 %) as risk factors. The presence of OPMDs and a previous blue (20.9 %). Only 13 % of the participants had received
history of upper aerodigetive tract malignancy were identified as specific training on diagnostic techniques relevant to oral can-
risk factors for oral cancer by 64.8 and 73.6 % of the partici- cer and OPMDs during their study.
pants, respectively. Fewer participants were able to identify poor Knowledge scores were calculated for each participant and
diet (26.7 %), prolonged immunosuppression (30.3 %), sun ex- ranged from 3 to 31. The mean knowledge score was 15.6±
posure (24.2 %), and older age (37.3 %) as factors contributing 5.4. Knowledge scores of participants who encountered a pa-
to the development of oral cancer. tient with oral cancer or OPMDs during their practice/training
Regarding knowledge about the types of oral lesions/ or reported recent attendance of continuous professional de-
conditions that might transform to cancer, 93.3 % of the par- velopment courses about oral cancer were significantly higher
ticipants knew at least one OPMD. Leukoplakia was the best compared to other participants (p<0.05). In addition, recently
known OPMDs by the participants (66.4 %). Erythroplakia, graduate practitioners (<10 years) had significantly higher
chronic hyperplastic candidiosis, lichen planus/lichenoid le- knowledge scores (p<0.05). No significant association was
sions, actinic cheilitis, and submucous fibrosis were known found between knowledge scores and gender, age, or specialty
as being OPMDs by 44.2, 39.7, 33.2, 17.9, and 15.5 % of the (medical vs. dental) of participants (Table 1).
participants, respectively. Regarding early detection practices, only 17.8 % of the

Table 1 Factors associated with early detection practices of oral cancer, knowledge about oral cancer, and diagnostic ability of early cancer and oral
potentially malignant disorders

Interviewee variable No (%). Early detection practice p value Knowledge scoreb P value Diagnostic p value
scorea mean (± SD) mean (± SD) abilityc mean (± SD)

Gender M 233 (70.6) 11.5 (4.6) 0.50 15.4 (5.4) 0.19 41.1 (17.8) 0.45
F 97 (29.4) 11.2 (4.3) 16.3 (5.3) 42.8 (20.2)
Age (years) ≤30 117 (35.5) 11.5 (4.5) 0.82 15.8 (5.0) 0.16 44.1 (17.5) 0.62
31–40 113 (34.2) 11.3 (4.5) 14.9 (5.2) 42.3 (18.8)
>40 100 (30.3) 11.1 (4.6) 16.3 (6.0) 44.7 (20.4)
Specialty GDP 165 (50) 11.2 (4.5) 0.15 15.6 (5.6) 0.79 43.7 (19.3) 0.99
GMP 165 (50) 11.9 (4.5) 15.8 (5.2) 43.7 (19.6)
Experience (years of practice) <10 183 (55.5) 12.0 (4.5) 0.045 15.8 (4.8) 0.037 43.4 (18.4) 0.76
11–20 76 (23) 10.5 (4.5) 14.4 (5.6) 45.0 (18.4)
>20 71 (21.5) 11.5 (4.4) 13.6 (6.3) 42.9 (20.7)
Encountered a patient with Yes 163 (49.4) 12.2 (4.7) 0.016 17.2 (5.4) <0.001 49.8 (20.2) 0.026
oral cancer/OPMDs No 167 (50.6) 11.0 (4.3) 14.2 (5.0) 42.0 (17.5)
Attendance of continuous Yes 52 (15.8) 13.5 (3.8) 0.001 17.2 (4.9) 0.026 43.1 (19.9) 0.82
professional development No 278 (84.2) 11.2 (4.6) 15.4 (5.0) 43.8 (18.7)
course on oral cancer/OPMDs

SD standard deviation, OPMDs oral potentially malignant disorders, GDP general dental practitioner, GMP general medical practitioner
a
Early detection practice score ranges from 0-24
b
Knowledge score ranges from 0-31
c
Diagnostic ability out of 100 %. p value of Student’s t test
J Canc Educ

participants reported that they routinely performed oral cancer


screening. Nearly half of the participants (53 %) reported that
they inspect mucosal surfaces of the oral cavity every time
they encounter a new patient. Fewer participants however
claimed that they always palpate oral mucosal surfaces
(14.2 %), examine floor of the mouth/ventrolateral surfaces
of the tongue and the retromolar trigone (21.5 %), inspect the
oropharynx (33.6 %), and palpate cervical lymph nodes
(32.7 %).
While 62.1 % of the participants reported that they always
ask patients about smoking habits, only 25.8 % reported such
practice regarding alcohol consumption. Less than half of the
participants (46.1 %) routinely provided patients with
smoking cessation and alcohol moderation advice.
When asked about their action when they encounter a pa-
tient with a suspicious oral lesion, most participants (87.6 %) Fig. 1 Scatter plot showing correlation between knowledge about oral
would refer the patient to the appropriate specialty, 10.6 % cancer and potentially malignant disorders and early detection practices
would do biopsy, 0.9 % would wait and see, and 0.9 % would reported by participants. A significant positive correlation was found
between knowledge score and early detection practices score (r=0.22,
attempt to treat the patient. Most participants (81.2 %) agreed p<0.001)
that they would value further training in the diagnosis and
assessment of oral cancer and OPMDs. suspicious oral lesions and early detection practices (r=0.01;
Early detection practice scores were calculated for each p=0.92) (Fig. 2).
participant and ranged from 2 to 21. The mean early detection
practice score was 11.55±4.5. Early detection practice scores
of participants who had encountered a patient with oral cancer
or OPMDs during their practice/training or who reported re- Discussion
cent attendance for continuous professional development
courses about oral cancer were significantly higher compared The poor prognosis of much oral cancer has been largely at-
to other participants (p<0.05). In addition, participants with a tributed to delays in diagnosis and treatment [2]. Previous re-
relatively recent graduation (<10 years) had significantly search has indicated that opportunistic screening of oral muco-
higher scores compared to older graduates (p<0.05). No sig- sal surfaces by primary HCPs may lead to earlier diagnosis and
nificant association was found between early detection prac- greatly increases the probability of cure and the rate of survival
tice scores and gender, age, or specialty (medical vs. dental) of with minimum deformity and impairment [20]. Many oral can-
participants (Table 1). A significant positive correlation was cers are preceded by noticeable mucosal changes (OPMD);
found between knowledge scores and early detection practice this combined with the fact that the oral cavity is easily acces-
scores (r=0.22; p<0.001) (Fig. 1). sible for examination makes the early diagnosis of oral cancer a
Validated clinical images were shown to participants to reasonably achievable target. However, most oral cancers,
examine their ability to recognize suspicious oral lesions. Par- even in developed countries, are still detected at late stages
ticipants were asked to choose images that they would con- [21]. In the present study, we wanted to examine factors that
sider suspicious (i.e., represent cancer or OPMDs) from a influenced diagnosis of precancerous changes and early detec-
collection of 52 clinical images. The participants’ ability to tion of oral cancer in a sample of primary HCPs in Jordan.
recognize suspicious lesions ranged from 11.5 to 96.15 %, The findings of the present study revealed that most partic-
with a mean of 43.6±18.9 %. Participants who reported en- ipants were able to identify tobacco as a major risk factor for
countering patients with oral cancer or OPMDs during their oral cancer. Studies from both developed and developing
practice/training were significantly more capable of recogniz- countries have shown similar results, indicating that tobacco
ing suspicious oral lesions compared to other participants is a well-known risk factor for oral cancer among HCPs
(p<0.05). No significant association was found between abil- [4–16]. Similar to other studies, the association between alco-
ity to recognize suspicious lesions and gender, age, attendance hol consumption and oral cancer was less known, indicating
of continuous education courses, and specialty of participants that there is a need to educate health-care professionals about
(medical vs. dental) (Table 1). The ability of participants to the adverse effect of alcohol consumption on oral tissues [8,
recognize suspicious oral lesions significantly correlated with 15, 16]. In fact, only a minority of participants routinely asks
their knowledge scores (r=0.39; p<0.001). However, there their patients about alcohol consumption, and less than half of
was no significant correlation between ability to recognize the participants routinely provide patients with smoking and
J Canc Educ

Fig. 2 Scatter plot showing correlations between ability to recognize and knowledge score (r=0.39, p<0.001) (a). No significant positive
suspicious oral lesions and knowledge about oral cancer and potentially correlation was found between diagnostic ability and early detection
malignant disorders and early detection practices reported by participants. practices score (r=0.01, p=0.92) (b)
A significant positive correlation was found between diagnostic ability

alcohol cessation advice. Contrary to general beliefs, alcohol OPMDs. Alami et al., 2013 also examined oral cancer knowl-
is consumed by some Arab populations. HCPs should there- edge among recently graduated medical and dental profes-
fore be encouraged to inquire about risk habits such as sionals from Jordan and found that the knowledge of recently
smoking and alcohol consumption and provide patients with graduate dentists is significantly better compared to recently
professional counseling regarding smoking and alcohol ces- graduated medical practitioners [6]. In contrast to their find-
sation. This is particularly important in conservative commu- ings, we did not find a significant difference regarding the
nities, like Arab countries, where patients may understandably overall knowledge about oral cancer between medical and
be reluctant to disclose their habits, in particular alcohol con- dental practitioners; probably because our study included
sumption because of cultural and religious reasons. High-risk practitioners with variable ages and years of practice. It seems
HPV infection, particularly with HPV-16 and HPV-18, is con- that recently graduated practitioners have better factual knowl-
sidered an independent risk factor for a subset of oropharyn- edge because they still retain information they were taught
geal cancers [22]. More than half of the participants in the during their undergraduate study. This knowledge however
present study were unaware of this fact; a figure similar to that is gradually lost over time through memory decay. The results
reported findings in other studies [4, 6, 8]. In addition, the of our study support this notion because it shows that relative-
majority of participants were unaware of the association be- ly, recently graduated (<10 years) participants had significant-
tween poor diet, prolonged sun exposure, immunosuppres- ly better knowledge compared to practitioners with less recent
sion, and older age with the development of oral cancer. These graduation. These findings also support the importance of
findings suggest that there is a defect in the knowledge of continuous professional development courses in maintaining
HCPs regarding risk factors of oral cancer, a factor that might practitioners’ knowledge current and updated.
limit their ability to identify at risk patients and take appropri- The present study examined the thoroughness of oral ex-
ate actions. Although a majority of the participants (64.8 %) amination performed by primary HCPs by using a series of
knew that oral cancer might develop from a precursor lesion, questions that probed specific examination procedures and the
only few knew the types, presentations, and diagnostic mo- frequency of performance. In contrast to studies from UK and
dalities of these lesions. For example, more than half of the USA, our study revealed that only a minority of participants
participants had no idea that erythroplakia is a OPMD, despite routinely perform oral cancer screening during their practice
this lesion having the highest risk of malignant transformation [4, 5, 7, 9]. In addition, common sites of oral cancer develop-
[2]. It appears to be necessary to emphasize the teaching of ment such as floor of mouth, ventrolateral surfaces of the
potentially malignant soft tissue lesions through the under- tongue, retromolar trigone, and the oropharynx were often
graduate curriculum and to provide updating opportunities overlooked during oral examination. Systematic soft tissue
for HCPs to ensure that their knowledge about oral cancer screening is an area of professional practice which could be
and OPMDs. In fact, the results of our study showed that improved with further training. In fact, several good manuals
attendance of continuous professional development courses and protocols are available for this purpose [23, 24]. We have
is associated with better knowledge about oral cancer and suggested a BRULE^ for cancer diagnosis—an acronym based
J Canc Educ

on red or white lesion, ulcer, lump, and exceeding 3 weeks Jordan. Health-care authorities such as Ministry of Health,
duration [25]. Oral cancer educational materials should be Jordan Medical Council, and health faculties in Jordanian uni-
made available for primary HCPs to improve their diagnostic versities should place collaborative efforts to establish contin-
abilities for the early signs of oral cancer and other mucosal uous medical/dental education system tailored to the educa-
diseases. The results of our study support this notion by dem- tional needs of Jordanian health-care workers.
onstrating a significant positive correlation between attendance The present study possesses several limitations. Although
of continuous professional development courses on oral cancer the characteristics of the participants were comparable to the
and the thoroughness of examination performed by primary national workforce profile, the results may not fully reflect the
HCPs. knowledge and practices of all medical and dental practi-
Importantly, the present study is the first to examine the tioners. Further large scale studies are therefore needed. In
ability of primary HCPs to detect suspicious oral lesions using addition, clinical images used in the present study were vali-
a collection of clinical images. This method might be a prom- dated by a small group of oral medicine specialists from a
ising tool for the assessment of early detection practices and limited geographic distribution and did not contain data with
diagnostic abilities of HCPs because it overcomes the discrep- regard to the history or duration of the lesions. Validation of
ancy between what HCPs report to do and what they actually the clinical images by experts from different geographic dis-
do. However, further validation of the clinical images by in- tributions would be desirable. In addition, factors related to
ternational experts in the field is warranted. Nevertheless, our lesions themselves such as color, size, and surface character-
results showed that the participants have inadequate diagnos- istics might influence the selection process; this is under cur-
tic abilities with regard to oral cancer and OPMDs (mean= rent investigations by authors of the study.
43.6 %). The ability to recognize suspicious lesions was
strongly correlated with encountering a patient with oral can-
cer or OPMDs during practice or training. This finding sup- Conclusion
ports the use of case-based approach and multimedia such as
clinical videos and images in continuous education courses The present study demonstrated an inadequate level of knowl-
because these methods might be more effective in improving edge about oral cancer and OPMDs among primary HCPs,
practical skills such as oral cancer detection and screening. including knowledge about risk factors, presentations, and
Further studies however are needed to test this suggestion. diagnostic techniques. In addition, primary HCPs showed in-
In contrast to other studies, the present study found no adequate early detection practices and limited diagnostic abil-
significant differences between medical and dental practi- ities. Although oral cancer is relatively uncommon in Jordan,
tioners regarding their knowledge, early detection practices, inadequate knowledge and practices of PHCs might have se-
and diagnostic abilities [6, 11, 14]. This is surprising because rious consequences on affected individuals. Interventions to
dental practitioners are expected to spend a good portion of improve primary HCPs knowledge and practices related to
their undergraduate study in learning oral soft tissues pathol- early diagnosis of oral cancer, through improvement of under-
ogy including oral cancer and OPMDs; therefore, it is not graduate curriculum and provision of continuous professional
unreasonable to assume that dental practitioners would have development courses, are needed. The latter is mandatory in
better scores. Dental students’ knowledge about oral cancer is some countries, such as UK and USA.
mainly introduced in oral medicine and oral pathology courses
in the 4th and 5th years of study. The current teaching of oral
pathology and oral medicine in Jordan has been largely theo- Conflict of Interest The authors declare that they have no conflict of
retical with a very limited practical component. Similarly, interest.
medical students are briefly introduced to the topic of oral
cancer in the general surgery lectures in the 5th and 6th years
of their study, with little clinical exposure. Improvement of References
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