Knowledge of Oral Cancer Among Recently Graduated Medical and Dental Professionals in Amman, Jordan

Transcription

1 Knowledge of Oral Cancer Among Recently Graduated Medical and Dental Professionals in Amman, Jordan Arwa Yousef Alami, B.D.S., FDSRCS, M.Sc.; Rula F. El Sabbagh, B.D.S., J.D.B.; Abdelhameed Hamdan, B.D.S. Abstract: Oral cancer is a devastating disease, and despite advances in treatment, the survival rate remains low. Early diagnosis can improve survival and outcomes. Delayed referrals are often due to the inadequate knowledge of general health professionals. The aim of this study was to assess the knowledge of oral cancer among recently graduated dental and medical professionals interested in working in a cancer center in Amman, Jordan. The study was conducted using a questionnaire to assess the knowledge of risk factors and the ability to correctly identify the oral lesions most commonly associated with oral cancer. A total of 112 individuals completed the questionnaire. The results revealed an inadequate level of knowledge of oral cancer among the study population, with significant differences between the dental and medical professionals. This study suggests there is a need for improvement of the undergraduate curriculum in oral cancer in both medical and dental schools in Jordan and for the provision of postgraduate and continuing education on this topic. Dr. Alami is Consultant Maxillofacial Prosthodontist, King Hussein Cancer Center, Amman, Jordan; Dr. El Sabbagh is Consultant in Pediatric Dentistry, King Hussein Cancer Center, Amman, Jordan; and Dr. Hamdan is General Dentist, King Hussein Cancer Center, Amman, Jordan. Direct correspondence and requests for reprints to Dr. Arwa Yousef Alami, King Hussein Cancer Center, P.O. Box , Queen Rania Alabdullah Street, Amman 11814, Jordan; aalalami@khcc.jo. Keywords: oral cancer, oral medicine, hospital dentistry, continuing education, Jordan Submitted for publication 3/26/12; accepted 9/30/12 The incidence of oral cancers, including lip cancers, varies greatly across the globe. In Jordan, the incidence of newly diagnosed oral cavity and lip cancers is 1 percent of all new cancer cases per year, and the attributable mortality rate is 0.6 percent of all cancer deaths. The incidence is slightly higher in men than women. 1 In general, early detection and diagnosis improve the probability of cure and may decrease the likelihood and/or degree of facial deformity. 2 Despite advances in the management of oral cavity cancers and an increased understanding of its causes, survival rates have not improved over the last few decades, and the five-year survival rate approaches only 50 percent and only in the best cancer centers worldwide. 3 The natural history of the disease itself is mutilating and can severely affect the patient s quality of life. Oral cancer interferes with speech, mastication, and the ability to engage in social interactions. 3 Early detection and treatment can improve the outcomes from oral cancer and allow for a better quality of life. 3 Previous research has indicated that delayed referrals to the appropriate specialist are due to the inadequate knowledge of general health practitioners in regard to understanding the risk factors for oral cancer and recognizing the characteristic lesions. 4 Usually, patients with oral cancers are first seen by either a general medical or dental practitioner. Studies conducted in different parts of the world have demonstrated an inadequate level of knowledge about oral cancers among health professionals, including a lack of knowledge about risk factors and the proper examination techniques Studies conducted in developed countries, such as the United States, 5-7 Canada, 8 and countries in Europe, 9-12 as well as in developing countries, such as Saudi Arabia 13 and Kuwait, 14 have found an inadequate level of knowledge about oral cancer and the need to improve this knowledge for better patient outcomes. Clinical and epidemiological information about oral cancer in Jordan is formally introduced in the undergraduate curriculum for both medical and dental students. The aim of our study was to evaluate physicians and dentists interested in working in a cancer center for their knowledge of oral cavity cancers, including lip cancers, the associated risk factors, common appearance on physical exam, and the conditions that are most commonly associated with oral cancer Journal of Dental Education Volume 77, Number 10

2 Materials and Methods This study was granted Institutional Review Board approval at King Hussein Cancer Center (KHCC) in Amman, Jordan. KHCC is a specialized tertiary referral center and treats all cancers including oral cavity cancers. It offers training in various fields of cancer diagnosis, treatment, and management. The study used a survey prepared by the investigators and written in English (English proficiency is a requirement for applying at KHCC). The survey consisted of items validated by twenty medical and dental professionals not included in the present study. The survey included questions that assessed knowledge of predisposing factors, common sites, appearance of oral cancer, and conditions often associated with oral cancers. The survey tested twelve possible risk factors for oral cancer, six of which are considered true risk factors by the scientific evidence: tobacco, alcohol, HPV, low consumption of vegetables and fruit, sun exposure, and old age. Six of the risk factors have not been proven scientifically: obesity, hot beverages, poor oral hygiene, spicy food, poorly fitting dentures, and family history of cancer. The survey was distributed at the end of the hospital job entrance exam. Applicants gave their consent by answering the questionnaire, and no names were attached to avoid bias. The study population consisted of newly graduated medical and dental personnel applying for surgical posts at KHCC at the resident (senior house officer) level. Consequently, the sample size was determined by the number of health professionals applying to the surgery department at KHCC. A total of 112 candidates answered the questionnaire. The demographic characteristics of the residents, including gender, medical or dental degree, and graduation year, were assessed in the questionnaire. The demographic characteristics of the respondents, along with their answers to the questionnaire, were described as counts and percentages. A comparison of the answers provided by the two groups of respondents (dental and medical residents) was carried out using a chi-square or Fisher s exact test. A significance criterion of p<0.05 was used in the analysis. All analyses were performed using SAS 9.2 (SAS Institute Inc., Cary, NC). The statistical analysis was completed by the statistical unit at KHCC. Results Of the 112 respondents, twenty-six (23 percent) were females, eighty-two (73 percent) were males, and four did not report gender. Fifty-five respondents (49 percent) had a dental degree, and the remaining fifty-seven (51 percent) had a medical degree. The participants had an average of one to five years of postgraduate education. The majority knew that squamous cell carcinoma is the most common type of oral cancer, with 98.2 percent of the dental graduates and 89.3 percent of the medical graduates answering correctly. The majority of the respondents (92 percent) were also able to identify tobacco use as a significant risk factor for oral cancer, with no significant difference between the dental and medical school graduates responses. Only 39.6 percent of the respondents overall knew that the lesions associated with chewing tobacco resolve after tobacco cessation. Regarding risk factors for oral cancer, alcohol use was less likely to be correctly identified as a risk factor by the group as a whole, but dental graduates were significantly more likely to respond correctly (p=0.01). The dental graduates were even more likely to correctly identify sun exposure as a risk factor for lip cancer when compared with the medical graduates (p<0.0001). Human papilloma virus (HPV) was correctly identified as a risk factor for oral cancer by only 34 percent of the respondents, with more dental than medical graduates responding correctly (p<0.001). A low consumption of fruits and vegetables was correctly identified as a risk factor by only 28.6 percent of the respondents, with no significance between the professions. Finally, the medical graduates were more likely to incorrectly identify hot beverages and poor oral hygiene as risk factors for oral cancer (p< for both items). Percentages of respondents identifying risk factors are shown in Figure 1, and the non-risk factors are shown in Figure 2. The respondents knowledge concerning the diagnosis of oral cancer was assessed through several questions on lesion appearance, lymph nodes, and the most common sites for oral cancer. The majority of the dental respondents knew that oral cancers are usually diagnosed in the late stage of the disease; they were significantly more aware of this than the medical graduates (p<0.001). The majority of the combined respondents (90.2 percent) recognized the appearance of early oral cancer lesion and understood October 2013 Journal of Dental Education 1357

3 Figure 1. Percentage of respondents who correctly identified risk factors Figure 2. Percentage of respondents who correctly identified non-risk factors 1358 Journal of Dental Education Volume 77, Number 10

4 how to detect metastatic lymph nodes by answering yes to the question if metastatic lymph nodes were hard painless mobile or fixed. Most common conditions associated with oral cancer were also identified by the respondents. However, few of them knew that erythroplakia was associated with oral cancer (32 percent), with a significant difference between dental and medical respondents (p<0.001) (Table 1). Discussion Oral cancer is the tenth most common cancer in the world. 15 It is associated with one of the most dismal five-year survival rates of the major cancer types. Being aware of the major risk factors for oral cancer and its associated conditions and the ability to identify the early lesions of oral cancer are vital for both the prevention and early detection of the disease. 16 Researchers in oral cancer agree that early diagnosis greatly increases the probability of cure and the rate of survival with minimum impairment and deformity. 17 It is critical that both general medical and dental practitioners possess sufficient knowledge of the signs and symptoms of malignant and premalignant oral cavity lesions for the sake of early and effective diagnosis. It is generally believed that dental professionals are more likely to examine their patients for oral cancer as part of their routine dental exam. However, the population at greatest risk for oral and pharyngeal cancers is more likely to visit a physician than a dentist A study from the United Kingdom found that the individuals at greatest risk for oral cancer rarely visit a dentist but do consult general medical practitioners (GMPs) and thus concluded that GMPs could play an important role in the early detection of oral cancer. 10 Newly graduated medical and dental professionals will be faced with the challenge of examining patients who might have oral cancer, so their knowledge on this subject is critical for the accurate and timely diagnosis of and referral for this potentially life-threatening disease. Our study therefore investigated both medical and dental professionals who are qualified and interested in working in a cancer center where they will be expected to give advice about oral cancer and its prevention. Risk Factors Most oral cancers are attributed to the use of alcohol and tobacco in its various forms. In addition, there is evidence that squamous cell carcinoma is strongly correlated with HPV. Other risk factors include sun exposure for lip cancer, betel quid, and low consumption of fruits and vegetables for oral cancer overall Our study found that the majority of respondents, both medical and dental graduates, were able to identify tobacco as a risk factor for oral cancer. Previous studies in both developed and developing countries have shown similar results, indicating that tobacco use is well known throughout the health professions as a risk factor for oral cancer This knowledge could be used to educate newly graduated general practitioners about tobacco cessation programs that may help in decreasing the incidence of oral cancer. Another study concluded that dentists need to receive continuing education in oral cancer prevention and early detection and the importance of providing tobacco and alcohol cessation counseling. 25 A case-controlled study sought to assess the risk for oral cancer associated with poor oral hygiene and periodontal disease. 26 Both states of poor oral health can affect the oral biofilm, which may become more pathogenic. However, a recent meta-analysis of published epidemiologic studies found that no significant risk for oral cancer is conferred by poor oral hygiene. 3 Thus, in our study, poor oral hygiene was not considered a true risk factor for oral cancer. Nearly 63 percent of the medical respondents in our study thought that poor oral hygiene is a risk factor in oral cancer, which is similar to the findings from a previous study conducted in the United States with a population of family physicians. 27 These findings are concerning and suggest that inaccurate information may affect the clinical judgment of physicians and result in the distribution of inaccurate information regarding the risks for oral cancer. More than 100 types of HPV have been identified. In the oral cavity alone, HPV-6, -11,-16, -18, -31, -33, and -42 have been isolated. 28 High-risk HBV genotypes such as 16 and 18 and the presence of one or both are considered an independent risk factor or partial cause for oral cancer. 3 A recent meta-analysis of published studies of oral lesions reported a potentially causal association between high-risk HPV and oral cancer and other potentially malignant diseases such as leukoplakia and epithelial dysplasia. 28 In our study, we considered HPV as a risk factor for oral cancer. Only 34 percent of the respondents were able to correctly identify HPV as a risk factor, and the dental graduates were more likely to respond correctly. The increased consumption of leafy green vegetables was found to reduce the risk of oropha- October 2013 Journal of Dental Education 1359

5 ryngeal cancers in a previous study. 29 Additional recent observations have provided strong evidence that adequate dietary intake plays an important protective role in the development of all cancers, including oral cancer. 30 Thus, for the purpose of our study we considered the low consumption of fruits and vegetables a risk factor for oral cancer. Among our respondents, only 28.6 percent correctly identi- Table 1. Respondents answers to survey concerning early appearance and most common associated lesions and areas of oral cancer (n=112) Question Response Total Number Respondents Dental Number (%) Medical Number (%) The early oral cancer lesion is answer Asymptomatic (90.9%) 44 (78.6%) Symptomatic 17 5 (9.1%) 12 (21.4%) Most common form of oral cancer is SCC. answer (1.8%) 6 (10.7%) (98.2%) 50 (89.3%) Lesions associated with smokeless tobacco generally resolve after discontinuation of these products. answer (54.5%) 25 (45.5%) 1 37 (66.1%) 19 (33.9%) p-value Most oral cancer lesions are diagnosed in: stage answer <0.001 Early stage (24.1%) 28 (50.0%) Late stage (75.9%) 28 (50.0%) Most common area: lips (70.9%) 33 (57.9%) (29.1%) 24 (42.1%) Most common area: tongue (70.9%) 44 (77.2%) (29.1%) 13 (22.8%) Most common area: floor of mouth (54.5%) 38 (66.7%) (45.5%) 19 (33.3%) Tongue most common area: dorsum (76.4%) 44 (77.2%) (23.6%) 13 (22.8%) Tongue most common area: ventral (83.6%) 39 (68.4%) (16.4%) 18 (31.6%) Tongue most common area: lateral surface (38.2%) 32 (56.1%) (61.8%) 25 (43.9%) Clinical appearance of early cancer lesion is small painless red or white area. answer (5.5%) 52 (94.5%) 2 6 (10.9%) 49 (89.1%) Conditions associated: erythroplakia (52.7%) 47 (82.5%) < (47.3%) 10 (17.5%) Conditions associated: lichen planus (85.5%) 50 (87.7%) (14.5%) 7 (12.3%) Conditions associated: leukoplaki (60.0%) 20 (35.1%) (40.0%) 37 (64.9%) Conditions associated: nicotinic stomatitis (85.5%) 50 (87.7%) (14.5%) 7 (12.3%) Signs of lymph node most characteristic of oral cancer metastasis are a hard painless mobile or fixed lymph node. p 0.05 considered significant answer (20.0%) 44 (80.0%) 1 4 (7.1%) 52 (92.9%) Journal of Dental Education Volume 77, Number 10

6 fied the low consumption of fruits and vegetables as a risk factor for oral cancer, which may affect their ability to adequately advise their patients on following a healthier lifestyle. In a related question, nearly 40 percent of the respondents reported that a positive family history for cancer is a risk factor for oral cancer although this is a misconception. This finding is concerning for the respondents ability to correctly identify the highest risk populations for which oral cancer screening may be appropriate. When we combined the risk factors in our study, we classified the respondents who correctly identified five or more of the six risk factors for oral cancer as having a high level of knowledge; those who identified three or four risk factors had a moderate level of knowledge; and those who identified fewer than three risk factors had a poor level of knowledge. Our results showed that 40 percent of the dental respondents possessed a high level of knowledge of the risk factors for oral cancer, 36.4 percent possessed a moderate level of knowledge, and 23.6 percent possessed a poor level of knowledge. In contrast, only 8.8 percent of the medical respondents possessed a high level of knowledge, 49.1 percent possessed a moderate level of knowledge, and 42.1 percent possessed a poor level of knowledge. The knowledge gap between the dental and medical graduates was significant (p= ). The findings from this study thus suggest that newly graduated general dental practitioners are more knowledgeable about risk factors of oral cancer than newly graduated general physicians, which is consistent with the findings from a similar study conducted in Italy. 31 Knowledge About Oral Cancer The majority of our study population could recognize the appearance of early cancer lesions and of metastatic lymph nodes, but the study did not investigate if the respondents were able to apply their theoretical knowledge to their clinical practice. In terms of the respondents knowledge of the most common precancerous oral conditions that predispose to oral cancer, the study found that only 32 percent of the respondents knew that erythroplakia is associated with oral cancer. This lack of knowledge may lead to a delay in diagnosis and in obtaining oral biopsies when needed. Few of the respondents were able to correctly identify the tongue and floor of the mouth as the most common sites for oral cancer lesions, with 26 percent and 39.2 percent of the graduates correctly identifying each site, respectively. This lack of knowledge may limit the efficacy and sensitivity of an oral exam. Overall, there was a significant difference in the level of knowledge about oral cancer between the medical and dental graduates, with the dental graduates showing a much better command of the relevant information. This may be attributable to the fact that an undergraduate curriculum at a dental school is more likely to specifically address the topic of oral cancer. It may also be due to the fact that the study population of dental graduates was specifically interested in working at an oral surgery unit in a cancer hospital, indicating a greater propensity on their part to become knowledgeable about oral cancer. However, despite this expectation, the dental graduates demonstrated knowledge was not at a sufficient level, and the finding of inadequate knowledge among these dentists did not differ from studies in other countries where the study population did not work in a cancer center. When we examined whether knowledge of oral cancer changes with the number of years spent working in one s health-related field, we found there was no significant difference in level of knowledge between respondents with different levels of experience (Table 2). This suggests that any knowledge of oral cancer is obtained during undergraduate study and that there was no continuing education on this topic. In contrast, a study conducted in Kuwait found that dentists with fewer years of experience were more knowledgeable than those with more experience. 14 Both studies indicate the importance of continuing medical education and the need for postgraduate courses and seminars in oral cancer and health. Oral Cancer Education The participants in our study were asked if they had previously attended any courses on oral cancer, and only two respondents answered in the affirmative. This finding may be because few relevant postgraduate courses were offered, the practitioners were unaware of their existence, or the practitioners were simply not interested in the topic of oral cancer. Regardless, there must be a greater effort to encourage the provision and utilization of oral cancer education opportunities. Even though the population in our study consisted of health professionals who were interested in pursuing careers in the field of cancer medicine, we found that both the dental and general practitioners had limited information on oral cancer. This suggests October 2013 Journal of Dental Education 1361

7 Table 2. Respondents knowledge of risk factors compared with years of experience Obesity Respondents Years of Experience Total 5 Years 4 Years 3 Years 2 Years 1 Year p-value for chisquare Fisher s exact test p-value answer (100%) 13 (92.9%) 23 (100%) 52 (91.2%) 6 (85.7%) (7.1%) 0 5 (8.8%) 1 (14.3%) Sun exposure 66 2 (40.0%) 12 (85.7%) 11 (47.8%) 34 (58.6%) 2 (28.6%) (60.0%) 2 (14.3%) 12 (52.2%) 24 (41.4%) 5 (71.4%) Alcohol (42.9%) 5 (21.7%) 17 (29.3%) 1 (14.3%) (100%) 8 (57.1%) 18 (78.3%) 41 (70.7%) 6 (85.7%) Hot beverages 83 5 (100%) 11 (78.6%) 19 (82.6%) 39 (67.2%) 5 (71.4%) (21.4%) 4 (17.4%) 19 (32.8%) 2 (28.6%) Poor oral hygiene 61 3 (60.0%) 9 (64.3%) 15 (65.2%) 28 (48.3%) 4 (57.1%) (40.0%) 5 (35.7%) 8 (34.8%) 30 (51.7%) 3 (42.9%) Spicy food 85 3 (60.0%) 11 (78.6%) 18 (78.3%) 46 (79.3%) 4 (57.1%) (40.0%) 3 (21.4%) 5 (21.7%) 12 (20.7%) 3 (42.9%) Poor-fitting dentures (80.0%) 1 (20.0%) 10 (71.4%) 4 (28.6%) 17 (73.9%) 6 (26.1%) 40 (69.0%) 18 (31.0%) 4 (57.1%) 3 (42.9%) HPV 74 3 (60.0%) 8 (57.1%) 18 (78.3%) 38 (65.5%) 2 (28.6%) (40.0%) 6 (42.9%) 5 (21.7%) 20 (34.5%) 5 (71.4%) Tobacco (7.1%) 2 (8.7%) 4 (6.9%) 2 (28.6%) (100%) 13 (92.9%) 21 (91.3%) 54 (93.1%) 5 (71.4%) Age >60 years 51 3 (60.0%) 9 (64.3%) 8 (34.8%) 26 (44.8%) 1 (14.3%) (40.0%) 5 (35.7%) 15 (65.2%) 32 (55.2%) 6 (85.7%) Low consumption of fruits and vegetables Familial history of cancer p 0.05 considered significant (100%) 0 2 (40.0%) 3 (60.0%) 11 (78.6%) 3 (21.4%) 7 (50.0%) 7 (50.0%) 20 (87.0%) 3 (13.0%) 12 (52.2%) 11 (47.8%) 38 (65.5%) 20 (34.5%) 19 (32.8%) 39 (67.2%) 3 (42.9%) 4 (57.1%) 1 (14.3%) 6 (85.7%) a need for better education in the diagnosis and treatment of oral diseases and for improvement in the oral health training curriculum in dental and medical education, as has been noted in other studies. 32,33 While one may expect to find significant differences between developed and developing countries in their practitioners awareness of a complex disease like oral cancer, none has been found in various studies Among proposals for a basic curriculum in oral pathology and medicine, the General Dental Council in the United Kingdom proposed guidelines for establishing learning outcomes in the fields of oral pathology and oral medicine. 34,35 Training that familiarizes general medical practitioners with the more common and important oral diseases may enhance their diagnostic abilities. This study does have possible limitations because it was conducted with a group of health care professionals seeking employment at one institution. The conclusions may therefore not be representative of all new medical and dental graduates, in Jordan or elsewhere. However, the findings may be more generalizable to candidates interested in working in a cancer center because KHCC is the only cancer center in Jordan. The results of our study suggest that there is a need in Jordan as reported in other countries for increased medical and dental curricular emphasis on the early signs and symptoms of oral malignancies to raise the level of knowledge about risk factors and associated oral and premalignant lesions among general health practitioners and dentists. Preventive 1362 Journal of Dental Education Volume 77, Number 10

8 activities, such as educating patients about the risks associated with the etiological factors of the disease and smoking cessation counseling, need to be emphasized to enable health professionals to help their patients make choices for a healthier lifestyle. Conclusions Our study found that these recently graduated medical and dental professionals were inadequately knowledgeable about oral cancer and their knowledge did not improve with the number of postgraduate years, either due to a lack of postgraduate courses on the subject or a lack of interest by the general practitioners. Other studies have demonstrated that the level of knowledge about oral cancer does not differ between developed and developing countries, nor does knowledge improve with the number of years spent practicing as a generalist. There is a need to improve the knowledge about oral cancer among health professionals worldwide, by ensuring that the material is taught as a critical part of dental and medical training and by ensuring that the relevant postgraduate and continuing education courses are made available. The current lack of awareness about oral cancer among general practitioners remains a significant barrier to prevention, early diagnosis, and lifesaving and life-improving intervention. REFERENCES 1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. GLOBOCAN 2008 cancer incidence and mortality worldwide. IARC CancerBase. 10. Lyon, France: International Agency for Research on Cancer, Joseph BK. Oral cancer: prevention and detection. Med Princ Pract 2002;11: Johnson NW, Warnakulasuriya S, Gupta PC, Dimba E, Chindia M, Otoh EC, et al. Global oral health inequalities in incidence and outcomes of oral cancer: causes and solutions. Adv Dent Res 2011;23: Schnetler JFC. Oral cancer diagnosis and delays in referral. Br J Oral Maxillofac Surg 1992;30: Patton LL, Elter JR, Southerland JH, Strauss RP. Knowledge of oral cancer risk factors and diagnostic concepts among rth Carolina dentists: implications for diagnosis and referral. J Am Dent Assoc 2005;136: Alonge OK, Narendran S. Oral cancer knowledge and practices of dentists along the Texas-Mexico border. J Cancer Educ 2004;19: Gajendra S, Cruz GD, Kumar JV. Oral cancer prevention and early detection: knowledge, practices, and opinions of oral health care providers in New York State. J Cancer Educ 2006;21: Clovis JB, Horowitz AM, Poel DH. Oral and pharyngeal cancer: knowledge and opinions of dentists in British Columbia and va Scotia. J Can Dent Assoc 2002;68: Lopez-Jornet P, Camacho-Alonso F, Molina-Miano F. Knowledge and attitudes about oral cancer among dentists in Spain. J Eval Clin Pract 2010;16: Carter LM, Ogden GR. Oral cancer awareness of general medical and general dental practitioners. Br Dent J 2007;203:E Hertrampf K, Wiltfang J, Koller M, Klosa K, Wenz HJ. Dentists perspectives on oral cancer: a survey in rthern Germany and a comparison with international data. Eur J Cancer Prev 2010;19: Colella G, Gaeta GM, Moscariello A, Angelillo IF. Oral cancer and dentists: knowledge, attitudes, and practices in Italy. Oral Oncol 2008;44: Jaber L, Shaban S, Hariri D, Smith S. Perceptions of health care practitioners in Saudi Arabia regarding their training in oral cancer prevention and early detection. Int J Health Care Qual Assur 2011;24: Joseph B, Sundaram D, Sharma P. Oral cancer awareness among dentists in Kuwait. Med Princ Pract 2012;21: Boyle P, Levin B. World cancer report. Lyon, France: IARC Press, Bloom B, Gift HC, Jack SS. Dental services and oral health: United States Vital Health Stat 1992;10: Goodman HS, Yellowitz JA, Horowitz AM. Oral cancer prevention: the role of family practitioners. Arch Fam Med 1995;4(7): Wade J, Smith H, Hankins M, Llewellyn C. Conducting oral examinations for cancer in general practice: what are the barriers? Fam Pract 2010;27: Joseph BK. Oral cancer: prevention and detection. Med Princ Pract 2002;11(Suppl 1): Moreno-López A, Esparza-Gómez G, González-Navarro A, et al. Risk of oral cancer associated with tobacco smoking, alcohol consumption, and oral hygiene: a case-control study in Madrid, Spain. Oral Oncol 2000;36: Statistics NCHS. Physicians contacts by sociodemographic and health characteristics, Vital Health Statistics, vol. 10. Washington, DC: U.S. Government Printing Office, Zain B. Cultural and dietary risk factors of oral cancer and precancer: a brief overview. Oral Oncol 2001;37: Horowitz A, Drury T, Goodman H, Yellowitz J. Oral pharyngeal cancer prevention and early detection: dentists opinions and practices. J Am Dent Assoc 2000;131: La Vecchia C, Tavani A, Franceschi S, Levi F, Corrao G, Negri E. Epidemiology and prevention of oral cancer. Oral Oncol 1997;33: Bloom B, Gift HC, Jack SS. Dental services and oral health: United States Vital Health Stat 1992;10: Guha N, Boffetta P, Filo BW, et al. Oral health and risk of squamous cell carcinoma of the head and neck and esophagus: results of two multicentric case-control studies. Am J Epidemiol 2007;166: Canto M, Horowitz A, Drury T, Goodman H. Maryland family physicians knowledge, opinions, and practices about oral cancer. Oral Oncol 2002;38: October 2013 Journal of Dental Education 1363

9 28. Meurman J. Infectious and dietary risk factors of oral cancer. Oral Oncol 2010;46: Sardella A, Demarosi F, Lodi G, Canegallo L, Rimondini L, Carrassi A. Accuracy of referrals to a specialist oral medicine unit by general and medical and dental practitioners and the educational implications. J Dent Educ 2007;71(4): Warnakulasuriya S. Significant oral cancer risk associated with low socioeconomic status. Evid Based Dent 2009;10: Syrjanen S, Lodi G, von Bultzingslowen I, et al. HPV infection in oral cancer and potentially malignant disorders. Oral Dis 2011;17: Pavia M, Pileggi C, bile CGA, Angelillo IF. Association between fruit and vegetable consumption and oral cancer: meta-analysis of observational studies. Am J Clin Nutr 2006;83: McCann PJ, Sweeney MP, Gibson J, Bagg J. Training in oral diseases, diagnosis, and treatment for medical students and doctors in the United Kingdom. Br J Oral Maxillofac Surg 2005;43: Macpherson LMD, McCann MF, Gibson J, Binnie VI, Stephen KW. The role of primary health care professionals in oral cancer prevention and detection. Br Dent J 2003;195: General Dental Council. The first five years: a framework for undergraduate education. 2 nd ed., At: Accessed: March 26, Journal of Dental Education Volume 77, Number 10