General dentists' knowledge, perceptions, and practices regarding oral potentially malignant disorders and oral cancer in Indonesia

Abstract Introduction The most effective means for reducing oral cancer (OC) mortality is by preventing late‐stage disease. Early diagnosis can be improved by increasing awareness among healthcare providers, specifically general dental practitioners (GDP). Therefore, our study aimed to assess GDPs' knowledge of OC risk factors and perceived competence in performing conventional oral examination (COE) in routine dental practice. Material and Methods This was a cross‐sectional study conducted in five provinces of Indonesia, namely: Aceh, Banda Aceh (BA); Bandung, West Java (WJ); special district Jakarta (JKT), JKT; Pontianak, West Kalimantan (WK); and Sorong, West Papua (WP). The local Dental Association or Faculty of Dentistry invited the GDPs to attend an education program and complete the survey. Results One hundred seventy‐seven GDPs completed the survey (WJ, n = 63; BA, n = 44, JKT, n = 27; WP, n = 23; and WP, n = 20). A large proportion (164 out of 177, 92.66%) of GDPs felt they had received insufficient training to equip them to diagnose OC and as many as 22.6% (n = 40) did not refer to specialists when they found suspicious mucosal lesions. Notwithstanding the significant regional variations, the majority of Indonesian GDPs self‐reported inadequate knowledge and awareness of OC and scarce confidence in performing COE. Conclusion GDP knowledge of OC risk factors and COE is key to improving early diagnosis of OC at a community level. Therefore, it is suggested that the lack of knowledge and confidence of GDPs reported here should be addressed through the national dental curriculum in Indonesia.


| INTRODUCTION
Detection of subjects with oral potentially malignant disorders (OPMDs) may facilitate an early diagnosis of oral cancer (OC), with consequent reduction of cancer burden (Mortazavi et al., 2014).Latestage OC is associated with significant morbidity and mortality.In contrast, early-stage OC has a favorable prognosis, with a 5-year survival rate of 66%-85% of individuals without regional lymph node involvement (Sciubba, 2001).Disappointingly, almost half of the patients with OC experience diagnostic delay and over 50% present with advanced-stage disease (Gonzalez-Moles et al., 2022).Thus, early diagnosis of OC is key, with the detection of an OPMD an important preventive measure to reduce the morbidity and mortality for OC (Warnakulasuriya et al., 2007).The estimated global prevalence of potentially malignant disorders of the oral cavity is approximately 1%-5% (Petti,2003), and these share some common OC risk factors such as smoking and betel quid chewing.
Unfortunately, no accurate data exists on the prevalence of OPMD in Indonesia.Rates of OC are also uncertain given the lack of a comprehensive national cancer registration system.Therefore, we previously conducted a pilot study to perform OC screening in Indonesia, where OPMDs were detected in 11.12% of participants and 0.2% had oral malignancy (Sari et al., 2017).More recently, the Global Burden of Disease (GBD) study reported an age-standardized incidence rate of lip and oral cavity cancer of 5.3 per 100,000 for Indonesia, which is likely an underestimation of the magnitude of the problem (Sari et al., 2023).One-third of Indonesians are tobacco smokers (about 87.3 million people) (Nurhasana et al., 2020;Soendoro, 2013;Wibowo et al., 2019), and areca nut chewing habits are a "heritage culture" passed down through many generations (Cheong et al., 2017;Fotlona, 2013).These lifestyle practices result in Indonesians having a high risk of developing malignancy, driving an increase in the incidence of OPMD and OC.
Several studies have reported that developed countries have relatively low rates of OC, while developing countries show higher rates in both females and males (Ferlay et al., 2010;Sharma & Om, 2015).
Further, improved health system infrastructure has the potential to curb OC mortality worldwide (Jemal et al., 2010;Sankaranarayanan et al., 1998).The increasing number of OC cases and unimproved 5year survival rate, therefore, could be due to several factors such as people's and practitioner's scarce awareness of OC.
General dental practitioners (GDPs) play a vital role in the detection of oral malignant and OPMDs.However, many GDPs fail to assess or diagnose OC and are not trained to detect early precursor lesions.The obstacles in undertaking a routine oral examination by GDPs have been recognized and include practitioners' lack of knowledge and experience (Gómez et al., 2010;Varela-Centelles et al., 2015).In addition, inadequate GDPs' skills, knowledge, and confidence to detect mouth cancer and precursor lesions may result in insufficient preventive education provided to their patients (Ford & Farah, 2013).GDPs' knowledge and awareness in recognizing early precursor lesions and educating patients, their ability to perform a complete examination and to appropriately refer patients have been shown to improve diagnostic delay and to decrease case fatality (Crossman et al., 2016;Gigliotti et al., 2019;Sankaranarayanan et al., 2002;Yellowitz & Goodman, 1995).
Given the importance of GDPs in OC early diagnosis and the lack of data regarding current practices of Indonesian GDPs, a study assessing their knowledge and awareness of OC and OPMD was warranted.We hypothesized that if a sizeable number of GDPs selfreported inadequate skills and confidence in performing OC early screening, a training intervention on OC screening could be beneficial to enhance GDP's knowledge, confidence, and ability to detect OPMD and OC earlier.
In the present study, we conducted a survey in diverse regions of Indonesia, namely Aceh, West Papua (WP), West Java (WJ); West Kalimantan (WK); and Central District of Jakarta (JKT).The aim of our study was to assess GDPs' knowledge of OC risk factors and their perceived competence in performing OC early screening in routine dental practice.The questions in the survey included GDPs' self-reported confidence in performing OC screening examination, knowledge of recognizing risk factors, and early signs of OC or OPMD.

| Study design
This was a descriptive cross-sectional study using a questionnaire survey.We adopted a multistage, stratified, cluster-sampling procedure, which considered geographical region, degree of urbanization, economic development status, gender and age distributions.The five cities selected for the study were: Banda Aceh (BA, Aceh), Bandung (WJ), JKT (special city district of Indonesia), Pontianak (WK), and Sorong (WP).

| Participant recruitment and sampling
The local Dental Association or Faculty of Dentistry invited the GDPs to attend a 1-day education program on oral malignant and OPMDs detection.The GDPs who attended the meeting obtained a clear explanation about the study and were given a copy of the plain language statement.The GDPs who consented were enrolled in the study after completing and signing an informed consent form.
Consecutive sampling was used as a technique in recruiting respondents and involved selecting all individuals who agreed to participate, provided they met pre-established criteria, until the desired number of subjects was recruited.

| Questionnaire
The questionnaire consisted of 43 questions developed from existing literature and modified to suit the local situation (Farah & McCullough, 2008;Mao, 2012;Maybury et al., 2012;Morse et al., 2011;Varela-Centelles et al., 2015).It underwent a validation process by a panel of senior researchers based in Indonesia to critically evaluate the suitability, clarity, simplicity, understanding, and sequencing of the questions (Appendix A).Following a pilot study that consisted of 10 Indonesian GDPs, appropriate modifications to the questionnaire were made before it was utilized in the main survey.The questionnaire consisted of multiple choice, open and closed questions, Likert scale including GDP's knowledge, awareness, attitude, subjective assessment of their clinical competence for screening of OC, and level of education.

| Data analysis
Completed questionnaire data were stored in the SurveyMonkey application.Data were exported to Microsoft Excel and were deidentified and coded to allow statistical analysis using Minitab Express© version 1.5.1.2017 and R commander.The difference between means was determined using multiway analysis of variance (ANOVA) followed by χ 2 and analyzing Likert scale results with logistic regression.Differences were considered significant where p < .05.

| Demographics of GDPs who participated in the study
The number of GDPs who enrolled in the education program and filled in the questionnaire was 177 (Table 1).The highest number of registered GDPs was from WJ region (n = 63), followed by BA (n = 44), JKT (n = 27), WP (n = 23), and WP (n = 20).Female respondents were predominant (n = 157, 88.7%).
More than half (50.28%) of the GDPs who enrolled in this study worked in community service.Slightly over a quarter (n = 48, 27%) of respondents worked in private dental practice, 9.6% (n = 17) worked in the dental teaching hospital, and the remainder worked in more than one location.
GDPs' workplace varied considerably depending on the region examined.In the WJ region, 93.85% GDPs who enrolled in this study worked in community service, whereas only 47.83% and 40% GDPs from WK and WP worked in community service, respectively.

| GDPs' awareness of OC in different Indonesian regions
GDPs' response toward questions related to their awareness of OC and OC training received at dental schools from each region varied considerably (Table 2).A large proportion (164 out of 177, 92.66%) of GDPs claimed to have received insufficient training to equip them to diagnose OC.All GDPs from WP (n = 20, 100%) felt they had insufficient training.A sizeable number of GDPs (8 out of 44, 18.18%) from BA felt they had received sufficient OC training at dental school (Table 2).
An overwhelming majority of GDPs (81.36%) admitted that they failed to educate their patients on OC risk factors.Eighteen out of 20 (90%) GDPs from WP reported to neglect educating patients and 90.48% GDPs from WJ did not educate patients either.
Over the whole five regions, 51.41% of GDPs indicated that they did not perform a screening on high-risk patients.In each region, there was some variation with 75% (15/20) and 61.9% (39/63) GDPs from WP and WJ reportedly skipping OC screening to high-risk patients.Conversely, 65.91%, 52.17%, and 59.26% GDPs from BA, WK, and JKT regions, respectively, undertook OC screening in highrisk patients.Similar responses were obtained for complete mouth examination (Table 2).Interestingly, 70.45% GDPs from BA region did not routinely perform a complete mouth examination, even | 3 of 11 though 65.91% reportedly undertook screening of high-risk patients.
This potentially contradictory response makes the screening results in high-risk patients questionable.

| Referral patterns
Overall, 22.6% (n = 40) of GDPs choose not to refer to specialists when they find suspicious mucosal lesions.13% (3 out of 23) and 30% GDPs (6 out of 20) from WK and WP, respectively, reported not to refer the patient with mucosal lesions.Furthermore, there were also few GDPs from urbanized regions, such as WJ (16 out of 63) and JKT (16 out of 27), who also elected not to refer patients with oral mucosal lesions despite the presence.Upon questioning regarding referral patterns after the recognition of suspected oral mucosal lesions, more than half of the GDPs (54.8%) indicated that they would refer to oral medicine (OM) specialists if they suspected their patients had either an OC or OPMD (Table 3).A sizeable number (n = 54, 29.94%) of GDPs did not know who best to refer their patients.
13.56% decided to send the patient to oral surgery and 1.13% to oral pathologist.As high as 75% (15 out of 20) of GDPs from WP responded that they do not know who to refer their patients.59.26% (16 out of 27) GDPs from JKT also responded they were confused as to whom to send the patients for further treatment.Conversely, all GDPs from BA reported knowing where to refer the patients, and most (90.91%) would send patients suspected with OC or OPMD to an OM specialist.

| GDPs' ability to perform COE and operative diagnostic techniques
There are eight steps to follow for a complete oral examination.The majority of GDPs claimed they performed COE steps, with the T A B L E 2 GDPs' response regarding OC in selected study regions.4).Only 2.84% (n = 5) GDPs from five selected provinces reported the ability to perform oral mucosal biopsy, 1.69% (n = 3) claimed to have the ability in applying toluidine blue staining procedure, and 2.26% (n = 4) the use of an adjunct light-based tool in OC early detection (Table 5).

| DISCUSSION
In the present study, we surveyed GDPs from five Indonesian provinces to assess their knowledge, perceptions, and practices regarding OPMDs and OC.Overall, our results show that GDPs feel  (Farah & McCullough, 2008;Varela-Centelles et al., 2015) as visual and tactile examination of a conventional oral examination that could detect early oral carcinoma (Irwin et al., 2011;Rethman et al., 2010;Varela-Centelles et al., 2015).
As part of OC prevention, educating patients regarding OC risk factors, particularly the major risk factors such as tobacco, areca nut, and alcohol, is of paramount importance.Also, it is desirable that patients receive adequate information about OC risk factors, especially from dental practitioners (Farah & McCullough, 2008;Maybury et al., 2012;Varela-Centelles et al., 2015).Disappointedly, our study revealed that most GDPs failed to educate patients on preventable lifestyle habits and behaviors that constitute OC risk factors.This has the potential to have a tremendous impact on OC incidence and prognosis in Indonesia.
More than half GDPs from the five studied regions admitted not performing a screening of high-risk patients.Many GDPs who worked in the front-line community service did undertake screening; however, they reported not to be sufficiently confident in performing these procedures.Notably, GDP/population ratio in Indonesia is 3.4 per 100,000 people (Rahardjo & Maharani, 2014;Soendoro, 2008Soendoro, , 2013)).
The limited number of GDPs in Indonesia poses considerable challenges to the oral healthcare system (Lazuardia et al., 2013;Soendoro, 2013).This shortage of human resources and the high demand for primary care might be a main reason for GDPs not performing a routine complete examination, particularly in high-risk patients.
Almost a quarter of GDPs do not refer to specialists when they observe suspicious lesions, potentially due to confusion as to whom they should refer.Remote regions in Indonesia have limited health facilities and specialist clinicians.However, there were also GDPs from WJ, BA, and JKT who did not routinely refer patients with OPMD or OC.This is more controversial as these regions are not considered remote and have more extensive health facilities compared to remote areas such as WK and WP regions.This could be due to a related lack of knowledge as to where best to refer for further treatment, but it is also possible that GDPs are not confident in diagnosing oral mucosal diseases and, when they suspect OPMD/ OC, are not familiar with the appropriate referral pathways for these patients (BDA, 2000;Mao, 2012;Morse et al., 2011;Varela-Centelles et al., 2015).GDPs from JKT also reported some confusion as to whom they should refer their patients for further treatment.In general, at a national level, there are only 3 dental specialists per 10,000 Indonesians (Rahardjo & Maharani, 2014;Soendoro, 2008), hence there is a need to improve dental health system and in particular the number of human resources.
The shortage of specialists together with dentists' privileged position as frontline dental professionals means that the burden of OC detection rests mostly with GDPs.The good news is that OC screening can be very effective with a simple visual examination (Sciubba, 2001).This can occur at a routine dental check or, in underserved areas, by screening that targets high-risk populations (Dwivedi et al., 2023).Sadly, research shows that general dentists feel ill-equipped and perform poorly when it comes to addressing suspicious lesions (Grafton-Clarke et al., 2019), and our study is in line with previous research.It would seem sensible, therefore, that the fight to reduce oral cancer mortality starts with a reform of dental and oral health curricula.In fact, lack of GDP's knowledge, skill, and awareness of performing OC screening is a common problem worldwide.Therefore, we suggest improving oral medicine curriculum with a more operative-clinical approach, where students can ideally assess more real-life cases directly and perform COE first hand.Further, case-based approach in the form of case-initiated and problem-based learning could increase students' understanding and skills in analyzing oral diseases.
In particular, COE should be included in a routine comprehensive examination that targets not only OC, but also oral diseases as a whole.The eight steps of COE by visual and tactile examination should be part of a routine clinical assessment in GDPs' daily practice.
The present study shows that whilst gingival examination was routinely undertaken, bimanual and floor of the mouth examinations were not.About half GDPs neglected tongue examinations.This is a worrisome finding, as these two areas are at high risk for the development of OPMD and could potentially develop into carcinoma (Mortazavi et al., 2014;Sreedhar et al., 2015;Warnakulasuriya et al., 2007).Hence, improvements are needed in the dental curriculum to equip students to undertake a proper clinical assessment of the oral mucosa and to recognize mucosal abnormalities, including OPMD and cancer.It is important to acknowledge, however, that there could be local and regional differences and/or specific areas of weakness in the dental curriculum and professional development.For example, a recent study assessing knowledge and practice regarding OC among dentists in JKT (Wimardhani et al., 2021) found that GDPs had a considerable level of knowledge of major risk factors of OC.However, the study highlighted that there were gaps especially in their perceived ability to perform diagnostic procedures.
This calls for action, particularly in improving dentists' competencies in operative procedures as well as background knowledge.

| CONCLUSION
GDPs have an important role in OC screening, however, most they are not adequately equipped to prevent, diagnose, and manage OC patients.Most GDPs fail to educate their patients about modifiable risk factors and do not perform screening in high-risk patients.With regional variations, a sizeable number of GDPs do not refer patients with suspected OPMD and OC.This was the first study surveying a sample of the Indonesian dentists across several provinces.More than half (50.28%) of the GDPs in the present study worked in community service or primary health care.The community service is the front-line health facility funded by the Indonesian government, where most individuals from middle and lower socioeconomic groups primarily seek care due to government subsidizing payment.Indonesian community services often lack good infrastructure, financial and human resources (Lazuardia et al., 2013; Rahardjo & Maharani, 2014).Dental practice and hospital are the second choice for people as they are much more expensive compared to community service.In remote areas, such as WP and WK, community service has a vital role for oral health.Most GDP respondents from JKT region (62.96%) and many from BA (40.91%) worked sometime in private dental practice, with only a few GDPs working exclusively in dental hospitals or general hospitals.In relation to OC curriculum training that was offered during their dental studies, the majority of GDP respondents in the present study felt they had received insufficient training on OC.This should be taken into consideration by the relevant planning and regulatory bodies, and the Indonesian Faculty of Dentistry may consider implementing OC training to allow GDPs to have adequate knowledge, skill, attitude, and confidence in a routine OC examination.Dental practitioners should remain aware of early sign and symptoms of cancer not confident 34.Do you perform a bimanual palpation on floor of the mouth?you believe you have the ability to perform an oral mucosal biopsy?a. Yes, If yes, have you performed an oral mucosal biopsy?Please circle the answer (Yes/No) b.No 38.Do you believe that you have the ability to perform Toluidine blue staining?a. Yes, where did you learn?please choose: you believe that you have the ability to use the adjunct tool for oral pre-cancer/cancer detection such as Velscope?a. Yes, where did you learn?Please choose: where will you refer them to?Please circle the answer (to Oral Medicine Specialist/oral Surgery/oral Pathology/ else _________________) b.No, as I have never suspected any of my patients to have had an oral malignant lesion.42.Will you refer your suspected patients with oral pre-malignant lesions?a. Yes If yes, where will you refer them to?Please circle the answer (to Oral Medicine Specialist/oral Surgery/oral Pathology/ else _________________) b.No, as I have never suspected any of my patients to have had oral pre-malignancy.43.What will you prescribe at the first appointment when you suspect a patient has an oral malignant or prenot give any medication and only do referral f.Other, please specify____________________________ T A B L E 4 COE steps done by GDPs.GDPs' ability to perform biopsy and adjunct tool.