Australian Dental Journal
The official journal of the Australian Dental Association
Australian Dental Journal 2015; 60: 397–403 doi: 10.1111/adj.12246
Patient perspectives of diagnostic delay for suspicious oral mucosal lesions K Allen,* CS Farah*† *UQ Centre for Clinical Research, The University of Queensland, Herston, Queensland. †The Australian Centre for Oral Oncology Research and Education, School of Dentistry, The University of Western Australia, Nedlands, Western Australia.
ABSTRACT Background: This study aimed to investigate patient experiences regarding the discovery of and subsequent referral for suspicious oral mucosal pathology. The population under investigation were patients of an oral medicine clinic in Australia who had been referred for oral lesions suspected for malignancy. Methods: A self-completed questionnaire gathered information regarding patient experiences and beliefs leading up to diagnosis at their review appointments. Results: Fifty-four per cent of participants knew about their mucosal pathology before referral. The highest proportion of delay occurred between self-discovery of a lesion and seeking help. Ninety-one per cent of self-aware participants had reason for seeking help in relation to their mucosal pathology. The three most common reasons for this was the desire for an explanation, being advised by a health care provider or presence of pain. Conclusions: Some patients were unaware of their own oral mucosal pathology and some seek help only when worried, in pain or following advice. Practitioners should examine the oral mucosa to detect suspicious oral mucosal pathology since patients may not be aware of its existence. Keywords: Awareness, mouth neoplasms, oral cancer, patients, survey. Abbreviations and acronyms: HCP = health care provider; HPV = human papillomavirus; OPMD = oral potentially malignant disorders; OSCC = oral squamous cell carcinoma. (Accepted for publication 15 October 2014.)
INTRODUCTION Oral cancer contributes approximately 2% of all new cancers diagnosed worldwide.1 Most oral cancers arise from oral epithelium in the form of squamous cell carcinoma. Oral squamous cell carcinoma (OSCC) is a rapidly progressing tumour, where treatment delay contributes to advanced stage at the time of treatment and hence increased morbidity and mortality.2 Oral potentially malignant disorders (OPMD) and early malignant lesions are usually asymptomatic. Often patients do not seek help for such lesions until signs or symptoms such as pain, ulceration, unexplained bleeding or a neck mass arise.3 Since obvious symptoms only present in late stages of malignancy, most oral cancers are relatively advanced at the time of diagnosis. Long-term survival of patients with oral cancer is dependent on the stage of disease at the time of diagnosis. Management of OPMD and early malignant lesions improves prognosis. Advanced lesions require © 2015 Australian Dental Association
more extensive surgery which leads to greater loss of tissue, resulting in permanent changes to appearance, oral function and communication.4 Improving quality of life post-treatment and reducing mortality from oral cancer is dependent on early detection and treatment. Oral mucosal screening serves to detect OPMD and OSCC at an early stage.5,6 Performing oral mucosal screening may not alter disease specific mortality; however, it can detect early lesions.5,6 Visual inspection is the primary strategy used for oral mucosal screening. Abnormalities in colour, texture, ulceration and persistent swelling with unknown aetiology may indicate malignancy.7,8 Diagnosis of OPMD and malignant oral mucosal lesions usually requires biopsy and histopathological assessment.7 These diagnostic procedures are best instituted by a professional trained in the field, such as an oral medicine specialist. Patient delay can occur at any of the stages which have been defined in the Anderson Model modified by 397
K Allen and CS Farah Walter et al.9 During the appraisal interval, patients will usually take time between recognizing a symptom to deciding to visit a health care provider (HCP).9 Reasons for taking time between recognition and decision can be attributed to their ideas about the lesion, or even attempts to self-medicate.10–12 During the help seeking interval, patients may take time between deciding to visit a HCP and scheduling an appointment due to their lifestyle factors, geographic location or availability of a HCP.9 Two studies noted that unmarried patients exhibit longer delay, both suggesting that this may be because married patients have more support.13,14 Social isolation is likely to impact on delay, as being unmarried can impact on social well-being in some cultures.14,15 Most patients report discussing their symptoms with their significant other.3 The most common oral symptoms noticed by a patient are a non-healing ulcer or sore, persistent lumps or swellings, sore tongue or mouth and sore throat, abscess or boil.3,16 Patients sometimes attribute these symptoms to an infection, dental problem or problem with a prosthesis.17 Those who believe their lesion to be innocuous will often wait longer to be seen by a HCP.3,11,17–19 One study hypothesized that patients who had previously experienced benign lesions may have a longer delay time, since they are less inclined to believe their condition needs attention.20 Of patients diagnosed with oral cancer, most can retrospectively pinpoint symptoms attributable to cancer and the majority of patients diagnosed with oral cancer report presenting as a result of their symptoms.10,21 This being said, symptom recognition is not a reliable method of detecting tumours at an early stage since about 25% of oral cancers remain asymptomatic until they reach an advanced size.22 Although tumours may not necessarily be detected at an early stage, attribution of symptoms to cancer can at least lead to earlier detection. Individuals who have had recent exposure to information regarding what symptoms require attention are less likely to exhibit delay.23 Finally there may be time taken during the diagnostic interval due to patient availability, beliefs or HCP guidance.9 Australian dental professionals value the importance of oral mucosal screening and are motivated to screen during dental examination.24–26 Most will refer suspicious oral mucosal lesions in a timely manner to appropriate specialists and many practitioners feel that their patients will not delay in having their lesions seen to by a specialist.24–26 This study was designed to report on the perspective of patients who have had suspicious oral mucosal pathology managed by an oral medicine specialist. The patients’ perspective can be understood by Australian dental professionals to gain an insight into how they might feel about their diagnostic journey. The purpose of this study was to quantify delay time 398
for suspicious oral mucosal lesions, to identify factors associated with delay between appointments and to ascertain patient beliefs and attitudes towards oral mucosal screening. METHODS A questionnaire was designed for this study to collect data from patients that had a history of suspicious oral mucosal pathology. Review of the literature was undertaken to formulate a questionnaire based on barriers and triggers to seeking help by oral cancer patients.27 Questions were framed in a manner that took into consideration qualitative statements that were provided by oral cancer patients in previous studies. Ethical clearance was granted by the University of Queensland Dental Science Research Ethics Committee. Trial questionnaires were completed by a set of pilot participants and questions were refined according to feedback. Reliability was assisted through test– retest of five participants and also through multiple questions that were designed to measure the same item. Retesting was set at least 6 months after the original test and results were compared for questions that should not be variable over time. Time intervals were also obtained from patient files to compare with self-reported time intervals. Questions that were not deemed reliable were removed from results and not interpreted. Validity was assisted through review of the literature, patient feedback and feedback from an oral medicine specialist (CSF). Participants were recruited from a private oral medicine clinic in Brisbane, Australia, where patients are specifically referred for oral mucosal pathology. Patients who were deemed suitable were invited to participate in the survey. No patients declined to participate. The clinic had a patient base that included maintenance patients under review for mucosal pathology in addition to newly referred patients. Patients who were seen in this clinic were referred for suspicious oral mucosal pathology which may or may not have been diagnosed as malignant. Lesions for which patients were referred were diagnosed by clinical and histopathological examination. This clinic was selected since it captured the sample population that this study aimed to investigate. Questionnaires were collected over 15 months from April 2012 to June 2013. Individuals who were seen by the clinic on the referral of a primary HCP (dentist, oral health therapist or doctor) were invited to participate in the study if they met eligibility criteria. To meet eligibility criteria, patients must have been referred for suspicious oral mucosal pathology. Patients were considered to have had suspicious oral mucosal pathology if they were referred for leukoplakia, erythroplakia or © 2015 Australian Dental Association
Patient perspectives on oral mucosal pathology erythroleukoplakia. Diagnosis of lesions was confirmed on clinical examination by an oral medicine specialist (CSF), and biopsy as required. Patients were not included if they could not consent or if they had difficulties with English language. Written consent was obtained from all participants. Participants were free to partially complete the survey, or to withdraw participation at any time during survey completion. A research assistant was available to assist participants on request during questionnaire completion. The testing instrument was a 32-item questionnaire which asked about regularity of dental visits, patient awareness of their lesion prior to mucosal screening, patient beliefs and attitudes about their mucosal lesion, triggers to help seeking, and beliefs and attitudes towards oral mucosal screening. Information was collected on gender, age, diagnosis of lesion, tobacco, alcohol and mouthrinse use. Most variables were dichotomized as ‘yes’ or ‘no’ answers while others were open text. Results are shown as percent agreement for any particular item unless otherwise specified. Correlations were tested with contingency tables using chi-square tests. RESULTS Data were collected from 101 participants. After checking for missing data, 16 were excluded as their questionnaires were less than 80% complete. A sample size of 85 was used in the final analysis for this study. Patient characteristics are shown in Table 1. There was a median of 4.5 years and a mean of 4.6 years between original referral for mucosal pathology and survey completion (actual time data available for 70 patients). Questionnaire results regarding participant beliefs about their mucosal pathology and oral cancer are shown in Table 2. Participants were asked in an open-ended question what they believed caused oral cancer and the three most common answers were smoking, drinking and poor oral hygiene. The 52.9% of participants who knew about their mucosal pathology before referral were asked about their experiences. Of those who were self-aware, 95.6% reported ‘feeling’ something different and 64.4%% reported ‘seeing’ something different. The three most common signs and symptoms seen or felt were pain, a lump or ulceration. Eighty-four per cent of self-aware participants had reason for seeking help in relation to their mucosal pathology. The three most common reasons for this in order of prevalence was the desire for an explanation, being advised by a HCP or presence of pain. Participants were asked in an open-ended question regarding how loved ones reacted after being told about their mucosal pathology. The three most common themes of advice given © 2015 Australian Dental Association
Table 1. Patient characteristics
Age 60 Gender Male Female Lesion diagnosis Dysplasia Oral lichen planus Hyperkeratosis only Lichenoid lesion OSCC Chronic hyperplastic candidosis Epithelial hyperplasia only Actinic cheilitis Epithelial hyperplasia with hyperkeratosis Other (chronic ulceration (1), amalgam tattoo, angiogranuloma, florid geographic tongue) Smoking status Current Past Never Regular alcohol consumption Yes No
n
%
38 47
44.7 55.3
38 47
44.7 55.3
34 11 9 8 8 4 3 3 2 4
40.0 12.9 10.6 9.4 9.4 4.7 2.4 3.5 2.4 4.7
21 31 33
24.7 36.5 38.8
63 22
74.1 25.9
in order of prevalence were to promote help seeking, to promote following the advice of a HCP, and to show concern or empathy. Four participants quoted in their open text boxes ‘everyone gets ulcers sometimes’, ‘just a mouth ulcer’, ‘interested, asked questions, said it would be ok’ and ‘don’t worry’ when asked what advice was given by loved ones regarding their mucosal lesions. Patient anxiety about checks for oral mucosal pathology are reported in Table 3. Patients who reported feeling anxious were asked to give reasons for feeling anxious and the most common reason was fear of detection. The reported amount of time elapsed between appointments is presented in Table 4. The highest proportion of delay occurred between self-discovery of a lesion and seeking help. This question had a response rate of 77.8% by self-aware patients for the question ‘How long between finding your oral condition did you get it checked’ and 87.1% by all patients for time intervals between first visit and referral, and the time interval between referral and specialist visit. Actual referrals to specialist visit time intervals were available for 69 patients. Patients had a median of 20 days and a mean of 28.7 days between referral to first visit at a specialist. For patients for which data were available who had also self-reported time between referral to first visit (n = 54), 50% reported their actual time interval correctly to within 2 weeks, 27.8% had overestimated their actual time interval by at least 2 weeks and 22.2% had underestimated their actual time interval by at least 2 weeks. 399
K Allen and CS Farah Table 2. Questionnaire results
Table 3. Anxiety about checks
Dental attendance related questions
Yes n
Do you see a dentist for regular 6 monthly check ups? Do you see a dentist when something needs fixing? Do you see the same dentist?
60
70.6%
-
-
25
29.4%
83
97.6%
-
-
2
2.4%
69
81.2%
-
-
16
18.8%
Lesion related questions
Yes n
Did you know about your lesion before screening? Did you feel it would get better with time? Did you feel it was normal? Did you feel it could be sinister? Have you experienced something similar in the past? Did you tell loved ones? Did you use products?
45
52.9%
-
-
40
47.1%
47
55.3%
1
1.2%
37
43.5%
18
21.2%
1
1.2%
66
77.6%
52
61.2%
0
0.0%
33
38.8%
16
18.8%
-
-
69
81.2%
Referral related questions
Yes n
Was it made clear why you were referred? Did you agree with your referral? Did you delay in using your referral?
84
98.8%
-
-
1
1.2%
83
97.6%
-
-
2
2.4%
6
7.1%
-
-
79
92.9%
Oral cancer related questions
Yes n
Have you heard of anyone who has had oral cancer? Should dentists be checking for oral cancer? Should doctors be checking for oral cancer? Is it beneficial for pamphlets? Beneficial for dentists to explain Beneficial for doctors to explain?
78
91.8%
-
-
7
8.2%
84
98.8%
-
-
1
1.2%
69
82.1%
-
-
15
17.9%
83
97.6%
-
-
2
2.4%
81
95.3%
-
-
4
4.7%
78
91.8%
-
-
7
8.2%
400
Unsure n
No n
Unsure n
How do you feel about checks?
n
%
Not anxious Slightly anxious Fairly anxious Very anxious Extremely anxious
49 14 15 4 3
57.6 16.5 17.6 4.7 3.5
Table 4. Patient reported time between appointments for mucosal pathology Time between discovery of lesion and seeking help n = 35* (%)
No n
Less than 2 weeks 2–4 weeks 1–3 months More than 3 months
Time between Time between first appointment referral being with health issued and first care provider appointment with and referral specialist being issued n = 74 (%) n = 74 (%)
12 (34.3%)
60 (81.1%)
35 (47.3%)
5 (14.3%) 8 (22.9%) 10 (28.6%)
3 (4.1%) 4 (5.4%) 7 (9.5%)
17 (23.0%) 17 (23.0%) 5 (6.8%)
*Only self-aware participants were included.
DISCUSSION 60
70.6%
-
-
25
29.4%
19
22.6%
-
-
65
77.4%
Unsure n
No n
Unsure n
No n
This study sought to understand patient experiences leading up to assessment and diagnosis of suspicious oral mucosal pathology. Information collected from participants increases understanding of the barriers and triggers to help seeking for oral mucosal pathology. Understanding experiences of patients referred for assessment of oral mucosal pathology can improve referral pathways and strategies. Most participants in the current study had heard of someone who had been diagnosed with oral cancer; however, this result is artificially high when compared with studies investigating the general public’s awareness of oral cancer.12,28 The results partly reflect an increased awareness of participants about oral cancer as attendees of an oral medicine clinic. The results of this study suggest that most patients are not anxious about receiving oral mucosal screening, although there were a minority of patients who reported anxiety. Of those who were anxious, worry was due to fear of finding oral cancer. The population under investigation had higher than normal awareness of oral cancer, thus they would be more aware of the devastation that a positive diagnosis would entail. It follows that there could be even less patient anxiety in the general population since oral cancer awareness is less prevalent. Further investigation into screening anxiety of the general population would be useful. Practitioners should educate patients on the relatively simple treatment of OPMD or early OSCC as opposed to late
© 2015 Australian Dental Association
Patient perspectives on oral mucosal pathology stage oral cancer. If patients understand the consequences of delaying mucosal screening, they may be motivated to seek regular examination. Studies have shown that oral mucosal screening is not always performed by dentists.29,30 Some dentists feel it is not their role to screen for mucosal pathology since they are not medical doctors. Patients will seek help where they expect that they will receive adequate care, and the results of our study suggest that most patients believe that both dentists and doctors should screen for mucosal lesions. Indeed, most patients also believed it would be beneficial for both dentists and doctors to explain what oral cancer was and how it could be caused. Most patients were aware of commonly known risk factors, such as smoking or drinking alcohol, however patients were largely unaware of the possible link between oral cancer and human papillomavirus (HPV).31 With the emergence of HPV associated oral cancer, it is of particular importance that patients are made aware of routes of HPV transmission. Educating patients on all oral cancer risk factors will enable them to assess their own oral cancer risk profile. While population based screening is not currently justified due to the relatively low prevalence of oral cancer, opportunistic screening, or targeting of groups known to be at higher risk for oral cancer may be more cost-effective.32 Opportunistic oral mucosal screening also provides an opportunity for the clinician to engage the patient in a discussion about oral cancer and enhance patient education about this disease and OPMDs generally. Most participants reported that dentists detected their oral mucosal lesion, while a small proportion of patients reported that oral health therapists or doctors detected their oral lesion. Patients with oral mucosal pathology may present to any health care setting, hence suitable educational material on this topic should be aimed at all primary HCPs. Many patients with symptomatic oral cancer will initially seek help with a doctor.33 Additionally, many patients who are at risk of oral cancer may not be regular dental attendees.34 This has implications for screening and referral protocols. Some dentists and doctors do not feel adequately trained to deal with oral mucosal pathology.30 Patients in this study expected that both dentists and doctors should check for and be able to explain oral mucosal pathology. The general public might expect similar standards of care. Adequate training for both dentists and doctors is required to meet patient expectations in this area. Most patients surveyed in this study were satisfied with the advice provided by their referring practitioner and most agreed to act on their referral. A very small proportion felt that they delayed their specialist appointment. Actual time and reported © 2015 Australian Dental Association
time between referral and first specialist visit was available for most (81.2%) patients. Actual and reported times were compared; this demonstrated that about half of patients were able to correctly record to within 2 weeks the actual time frame. Therefore, reliability of reported time frames by patients is questionable since about half were unable to report correctly the time frame and about a fifth did not record any time frame at all. Considering the median time between initial referral and survey completion of about 4.5 years, patients may be unable to accurately report time intervals due to recall bias. The median time of 20 days between referral and specialist visit shows that most patients will promptly visit a specialist when referred. The need for referring practitioners to communicate urgency to their patients when issuing a referral for oral mucosal pathology is to account for the minority of patients who delay in using their referral. Referring practitioners might also consider following up with patients subsequent to issuing a referral to ensure that patients are attending specialist appointments without delay. For cases that are highly suspicious for malignancy, practitioners should liaise with the specialist to ensure that the patient does not experience any undue delay due to difficulties securing an appointment. How a patient felt about their mucosal pathology did not have any correlation with the time taken between referral and first specialist visit. Perception of a serious condition that would not improve with time was also not correlated with whether a patient was diagnosed with OSCC or another oral mucosal lesion. Most participants perceived their condition as serious, since they felt that their lesion was not normal and that it could be something sinister. Those patients who did not feel that their condition was serious, or that their condition would get better with time were just as likely to promptly visit a specialist regarding their mucosal pathology. These results do not support the hypothesis that patients may delay affecting a referral if they do not believe that their condition is serious.35,36 This study was unable to identify a particular trait which could delay patient attendance to a specialist. This again emphasizes the importance of patient follow-up, as there may not be a particular referral communication strategy that will promote prompt use of a specialist referral. Patients in this study were generally satisfied with the advice that was given on referral, although what particular advice was provided was not investigated. Reasons for patient satisfaction with referrals would be useful to include in future studies, especially since in another study, a large proportion of patients were not happy with advice received upon their first medical consultation.3 The practitioner should be able to 401
K Allen and CS Farah gauge the patient’s emotional and social well-being to deliver medical information that the patient is able to comprehend.37 About half of the participants knew about their oral mucosal pathology prior to referral. This highlights the importance of clinicians visually examining the oral mucosa for abnormalities, since patients will not always present complaining of mucosal pathology. Even for those who were self-aware, some had lesions that were incidentally discovered by HCPs at appointments that were scheduled for other reasons (dental check-up or dental emergency). Most patients recalled ‘feeling’ something different and a smaller proportion remembered ‘seeing’ something different in their mouths. Presence of pain, seeking advice from a HCP, and seeking an explanation for the presence of oral symptoms were the most common reasons for seeking help in this study. Therefore, HCPs should enquire about changes noted by the patient relating to oral soft tissues. Most participants reported that loved ones had promoted help seeking, however a small proportion of participants recalled that loved ones advised them not to worry, or that their pathology was ‘just an ulcer’. Given that an ulcer is a common initial presentation that is remembered by oral cancer patients, greater public awareness about the significance of a nonhealing ulcer is required.3 The public know very little about the clinical presentation of oral cancer.38 Community awareness campaigns should focus attention of patients on seeking advice from a dentist if there are any changes in the appearance or sensation of their oral cavity. Patients are generally accepting of advice from HCPs. Promoting effective training among clinicians through continuing professional education will ensure that appropriate advice or referral is provided to patients, and delay is minimized. Practitioners who are not confident in their abilities might use telemedicine or electronic facilities to liaise with an oral medicine specialist for an opinion on the nature of the lesion and the need for referral. This study involved a group of patients who were referred to a private oral medicine specialist and may not capture the opinions of all individuals who have been referred for oral mucosal pathology. There are numerous referral pathways for patients with OSCC and OPMDs, including to an oral maxillofacial surgeon or an oral surgeon in either the private or public system. Future research to include these patients would be valuable to provide a better understanding on the issues that may impact on early detection of oral cancer. The small sample size, particularly of patients diagnosed with OSCC, means that these results are not generalizable. All due care was taken to ensure the self-reported questionnaire provided valid and reliable results, with data that was not considered reliable being removed. 402
CONCLUSIONS Most patient mediated delay occurred between selfdetection of a lesion and presentation to a primary HCP. Targeting this aspect of delay relies on raising community awareness about oral cancer. Many patients sought advice from loved ones prior to seeking help with a HCP and although most loved ones advised patients to seek help, there was still a small proportion who advised against it. Help seeking was delayed in these cases due to the belief that symptoms were normal. Considering that ulceration is a common presentation of OSCC, public perception that ulceration is normal may contribute to patient delay. Concern that oral mucosal screening creates patient anxiety was unfounded in this study, since most patients who were referred for suspicious oral mucosal pathology were amenable to being screened for oral mucosal pathology. Patients actually had an expectation that health professionals would perform mucosal screening and also explain what oral cancer is and how it is caused. Most patients interpreted their symptoms as something minor, even after being referred for suspicious pathology. Clinicians may be avoiding terminology that they believe will unnerve patients, as most patients were unaware of the potential significance of mucosal pathology. Clinicians should feel confident in discussing the presence of a suspicious lesion with their patients, since most patients were accepting of advice given by a HCP. AUTHORS’ CONTRIBUTIONS KA and CSF participated in study conception, design and data collection. KA performed the statistical analysis and drafted the manuscript. CSF checked results and edited the manuscript. The authors declare that they have no competing interests. ACKNOWLEDGEMENTS We thank the patients who participated in this study, the staff at the UQCCR (Fatima Dost and Lisa Dingwall) for assistance with questionnaire distribution and collection, and Dr Pauline Ford for assistance with questionnaire design. REFERENCES 1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010;127:2893–2917. 2. van der Waal I, de Bree R, Brakenhoff R, Coebergh JW. Early diagnosis in primary oral cancer: is it possible? Med Oral Patol Oral Cir Bucal 2011;16:e300–305. 3. Rogers SN, Vedpathak SV, Lowe D. Reasons for delayed presentation in oral and oropharyngeal cancer: the patients perspective. Br J Oral Maxillofac Surg 2011;49:349–353. © 2015 Australian Dental Association
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24. Allen K, Ford P, Farah C. Oral mucosal screening and referral attitudes of Australian oral health therapists and dental hygienists in Queensland. Int J Dent Hyg 2015;13:206–212. doi: 10.1111/idh.12103. 25. Allen K, Farah CS. Dental prosthetist experience with oral mucosal screening and referral. Quintessence Int 2014;45:891–897. 26. Allen K, Farah C. Screening and referral of oral mucosal pathology: a check-up of Australian dentists. Aust Dent J 2015; 60:52–58. 27. Farah CS, Ford PJ, Allen K, Vu AN, McCullough MJ. Oral cancer and potentially cancerous lesions – early detection and diagnosis. In: KUE Ogbureke, ed. Oral Cancer. ISBN: 978-95351-0228-1, InTech, doi:10.5772/30997. 28. Awojobi O, Scott SE, Newton T. Patients’ perceptions of oral cancer screening in dental practice: a cross-sectional study. BMC Oral Health 2012;12:55. 29. Klosa K, Wiltfang J, Wenz HJ, Koller M, Hertrampf K. Dentists’ opinions and practices in oral cancer prevention and early detection in Northern Germany. Eur J Cancer Prevent 2011;20:313–319. 30. Brocklehurst PR, Baker SR, Speight PM. A qualitative study examining the experience of primary care dentists in the detection and management of potentially malignant lesions. 1. Factors influencing detection and the decision to refer. Br Dent J 2010;208:E3; discussion 72-73. 31. Milbury K, Rosenthal DI, El-Naggar A, Badr H. An exploratory study of the informational and psychosocial needs of patients with human papillomavirus-associated oropharyngeal cancer. Oral Oncol 2013;49:1067–1071. 32. Speight PM, Palmer S, Moles DR, et al. The cost-effectiveness of screening for oral cancer in primary care. Health Technol Assess 2006;10:1–144, iii-iv. 33. Jovanovic A, Kostense PJ, Schulten EA, Snow GB, van der Waal I. Delay in diagnosis of oral squamous cell carcinoma; a report from The Netherlands. Eur J Cancer B Oral Oncol 1992;28B:37–38. 34. Frydrych AM, Slack-Smith LM. Dental attendance of oral and oropharyngeal cancer patients in a public hospital in Western Australia. Aust Dent J 2011;56:278–283. 35. Tromp DM, Brouha XD, Hordijk GJ, Winnubst JA, de Leeuw JR. Patient factors associated with delay in primary care among patients with head and neck carcinoma: a case-series analysis. Fam Prac 2005;22:554–559. 36. Morse DE, Velez Vega CM, Psoter WJ, et al. Perspectives of San Juan healthcare practitioners on the detection deficit in oral premalignant and early cancers in Puerto Rico: a qualitative research study. BMC Public Health 2011;11:391. 37. Newton JT. Reactions to cancer: communicating with patients, family and carers. Oral Oncol 2010;46:442–444. 38. Hertrampf K, Wenz HJ, Koller M, Wiltfang J. Public awareness about prevention and early detection of oral cancer: a population-based study in Northern Germany. J Craniomaxillofac Surg 2012;40:e82–86.
Address for correspondence: Professor Camile S Farah The Australian Centre for Oral Oncology Research and Education (ACORE) PO Box 88 RBWH Herston QLD 4029 Email: [email protected]
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The official journal of the Australian Dental Association
Australian Dental Journal 2015; 60: 397–403 doi: 10.1111/adj.12246
Patient perspectives of diagnostic delay for suspicious oral mucosal lesions K Allen,* CS Farah*† *UQ Centre for Clinical Research, The University of Queensland, Herston, Queensland. †The Australian Centre for Oral Oncology Research and Education, School of Dentistry, The University of Western Australia, Nedlands, Western Australia.
ABSTRACT Background: This study aimed to investigate patient experiences regarding the discovery of and subsequent referral for suspicious oral mucosal pathology. The population under investigation were patients of an oral medicine clinic in Australia who had been referred for oral lesions suspected for malignancy. Methods: A self-completed questionnaire gathered information regarding patient experiences and beliefs leading up to diagnosis at their review appointments. Results: Fifty-four per cent of participants knew about their mucosal pathology before referral. The highest proportion of delay occurred between self-discovery of a lesion and seeking help. Ninety-one per cent of self-aware participants had reason for seeking help in relation to their mucosal pathology. The three most common reasons for this was the desire for an explanation, being advised by a health care provider or presence of pain. Conclusions: Some patients were unaware of their own oral mucosal pathology and some seek help only when worried, in pain or following advice. Practitioners should examine the oral mucosa to detect suspicious oral mucosal pathology since patients may not be aware of its existence. Keywords: Awareness, mouth neoplasms, oral cancer, patients, survey. Abbreviations and acronyms: HCP = health care provider; HPV = human papillomavirus; OPMD = oral potentially malignant disorders; OSCC = oral squamous cell carcinoma. (Accepted for publication 15 October 2014.)
INTRODUCTION Oral cancer contributes approximately 2% of all new cancers diagnosed worldwide.1 Most oral cancers arise from oral epithelium in the form of squamous cell carcinoma. Oral squamous cell carcinoma (OSCC) is a rapidly progressing tumour, where treatment delay contributes to advanced stage at the time of treatment and hence increased morbidity and mortality.2 Oral potentially malignant disorders (OPMD) and early malignant lesions are usually asymptomatic. Often patients do not seek help for such lesions until signs or symptoms such as pain, ulceration, unexplained bleeding or a neck mass arise.3 Since obvious symptoms only present in late stages of malignancy, most oral cancers are relatively advanced at the time of diagnosis. Long-term survival of patients with oral cancer is dependent on the stage of disease at the time of diagnosis. Management of OPMD and early malignant lesions improves prognosis. Advanced lesions require © 2015 Australian Dental Association
more extensive surgery which leads to greater loss of tissue, resulting in permanent changes to appearance, oral function and communication.4 Improving quality of life post-treatment and reducing mortality from oral cancer is dependent on early detection and treatment. Oral mucosal screening serves to detect OPMD and OSCC at an early stage.5,6 Performing oral mucosal screening may not alter disease specific mortality; however, it can detect early lesions.5,6 Visual inspection is the primary strategy used for oral mucosal screening. Abnormalities in colour, texture, ulceration and persistent swelling with unknown aetiology may indicate malignancy.7,8 Diagnosis of OPMD and malignant oral mucosal lesions usually requires biopsy and histopathological assessment.7 These diagnostic procedures are best instituted by a professional trained in the field, such as an oral medicine specialist. Patient delay can occur at any of the stages which have been defined in the Anderson Model modified by 397
K Allen and CS Farah Walter et al.9 During the appraisal interval, patients will usually take time between recognizing a symptom to deciding to visit a health care provider (HCP).9 Reasons for taking time between recognition and decision can be attributed to their ideas about the lesion, or even attempts to self-medicate.10–12 During the help seeking interval, patients may take time between deciding to visit a HCP and scheduling an appointment due to their lifestyle factors, geographic location or availability of a HCP.9 Two studies noted that unmarried patients exhibit longer delay, both suggesting that this may be because married patients have more support.13,14 Social isolation is likely to impact on delay, as being unmarried can impact on social well-being in some cultures.14,15 Most patients report discussing their symptoms with their significant other.3 The most common oral symptoms noticed by a patient are a non-healing ulcer or sore, persistent lumps or swellings, sore tongue or mouth and sore throat, abscess or boil.3,16 Patients sometimes attribute these symptoms to an infection, dental problem or problem with a prosthesis.17 Those who believe their lesion to be innocuous will often wait longer to be seen by a HCP.3,11,17–19 One study hypothesized that patients who had previously experienced benign lesions may have a longer delay time, since they are less inclined to believe their condition needs attention.20 Of patients diagnosed with oral cancer, most can retrospectively pinpoint symptoms attributable to cancer and the majority of patients diagnosed with oral cancer report presenting as a result of their symptoms.10,21 This being said, symptom recognition is not a reliable method of detecting tumours at an early stage since about 25% of oral cancers remain asymptomatic until they reach an advanced size.22 Although tumours may not necessarily be detected at an early stage, attribution of symptoms to cancer can at least lead to earlier detection. Individuals who have had recent exposure to information regarding what symptoms require attention are less likely to exhibit delay.23 Finally there may be time taken during the diagnostic interval due to patient availability, beliefs or HCP guidance.9 Australian dental professionals value the importance of oral mucosal screening and are motivated to screen during dental examination.24–26 Most will refer suspicious oral mucosal lesions in a timely manner to appropriate specialists and many practitioners feel that their patients will not delay in having their lesions seen to by a specialist.24–26 This study was designed to report on the perspective of patients who have had suspicious oral mucosal pathology managed by an oral medicine specialist. The patients’ perspective can be understood by Australian dental professionals to gain an insight into how they might feel about their diagnostic journey. The purpose of this study was to quantify delay time 398
for suspicious oral mucosal lesions, to identify factors associated with delay between appointments and to ascertain patient beliefs and attitudes towards oral mucosal screening. METHODS A questionnaire was designed for this study to collect data from patients that had a history of suspicious oral mucosal pathology. Review of the literature was undertaken to formulate a questionnaire based on barriers and triggers to seeking help by oral cancer patients.27 Questions were framed in a manner that took into consideration qualitative statements that were provided by oral cancer patients in previous studies. Ethical clearance was granted by the University of Queensland Dental Science Research Ethics Committee. Trial questionnaires were completed by a set of pilot participants and questions were refined according to feedback. Reliability was assisted through test– retest of five participants and also through multiple questions that were designed to measure the same item. Retesting was set at least 6 months after the original test and results were compared for questions that should not be variable over time. Time intervals were also obtained from patient files to compare with self-reported time intervals. Questions that were not deemed reliable were removed from results and not interpreted. Validity was assisted through review of the literature, patient feedback and feedback from an oral medicine specialist (CSF). Participants were recruited from a private oral medicine clinic in Brisbane, Australia, where patients are specifically referred for oral mucosal pathology. Patients who were deemed suitable were invited to participate in the survey. No patients declined to participate. The clinic had a patient base that included maintenance patients under review for mucosal pathology in addition to newly referred patients. Patients who were seen in this clinic were referred for suspicious oral mucosal pathology which may or may not have been diagnosed as malignant. Lesions for which patients were referred were diagnosed by clinical and histopathological examination. This clinic was selected since it captured the sample population that this study aimed to investigate. Questionnaires were collected over 15 months from April 2012 to June 2013. Individuals who were seen by the clinic on the referral of a primary HCP (dentist, oral health therapist or doctor) were invited to participate in the study if they met eligibility criteria. To meet eligibility criteria, patients must have been referred for suspicious oral mucosal pathology. Patients were considered to have had suspicious oral mucosal pathology if they were referred for leukoplakia, erythroplakia or © 2015 Australian Dental Association
Patient perspectives on oral mucosal pathology erythroleukoplakia. Diagnosis of lesions was confirmed on clinical examination by an oral medicine specialist (CSF), and biopsy as required. Patients were not included if they could not consent or if they had difficulties with English language. Written consent was obtained from all participants. Participants were free to partially complete the survey, or to withdraw participation at any time during survey completion. A research assistant was available to assist participants on request during questionnaire completion. The testing instrument was a 32-item questionnaire which asked about regularity of dental visits, patient awareness of their lesion prior to mucosal screening, patient beliefs and attitudes about their mucosal lesion, triggers to help seeking, and beliefs and attitudes towards oral mucosal screening. Information was collected on gender, age, diagnosis of lesion, tobacco, alcohol and mouthrinse use. Most variables were dichotomized as ‘yes’ or ‘no’ answers while others were open text. Results are shown as percent agreement for any particular item unless otherwise specified. Correlations were tested with contingency tables using chi-square tests. RESULTS Data were collected from 101 participants. After checking for missing data, 16 were excluded as their questionnaires were less than 80% complete. A sample size of 85 was used in the final analysis for this study. Patient characteristics are shown in Table 1. There was a median of 4.5 years and a mean of 4.6 years between original referral for mucosal pathology and survey completion (actual time data available for 70 patients). Questionnaire results regarding participant beliefs about their mucosal pathology and oral cancer are shown in Table 2. Participants were asked in an open-ended question what they believed caused oral cancer and the three most common answers were smoking, drinking and poor oral hygiene. The 52.9% of participants who knew about their mucosal pathology before referral were asked about their experiences. Of those who were self-aware, 95.6% reported ‘feeling’ something different and 64.4%% reported ‘seeing’ something different. The three most common signs and symptoms seen or felt were pain, a lump or ulceration. Eighty-four per cent of self-aware participants had reason for seeking help in relation to their mucosal pathology. The three most common reasons for this in order of prevalence was the desire for an explanation, being advised by a HCP or presence of pain. Participants were asked in an open-ended question regarding how loved ones reacted after being told about their mucosal pathology. The three most common themes of advice given © 2015 Australian Dental Association
Table 1. Patient characteristics
Age 60 Gender Male Female Lesion diagnosis Dysplasia Oral lichen planus Hyperkeratosis only Lichenoid lesion OSCC Chronic hyperplastic candidosis Epithelial hyperplasia only Actinic cheilitis Epithelial hyperplasia with hyperkeratosis Other (chronic ulceration (1), amalgam tattoo, angiogranuloma, florid geographic tongue) Smoking status Current Past Never Regular alcohol consumption Yes No
n
%
38 47
44.7 55.3
38 47
44.7 55.3
34 11 9 8 8 4 3 3 2 4
40.0 12.9 10.6 9.4 9.4 4.7 2.4 3.5 2.4 4.7
21 31 33
24.7 36.5 38.8
63 22
74.1 25.9
in order of prevalence were to promote help seeking, to promote following the advice of a HCP, and to show concern or empathy. Four participants quoted in their open text boxes ‘everyone gets ulcers sometimes’, ‘just a mouth ulcer’, ‘interested, asked questions, said it would be ok’ and ‘don’t worry’ when asked what advice was given by loved ones regarding their mucosal lesions. Patient anxiety about checks for oral mucosal pathology are reported in Table 3. Patients who reported feeling anxious were asked to give reasons for feeling anxious and the most common reason was fear of detection. The reported amount of time elapsed between appointments is presented in Table 4. The highest proportion of delay occurred between self-discovery of a lesion and seeking help. This question had a response rate of 77.8% by self-aware patients for the question ‘How long between finding your oral condition did you get it checked’ and 87.1% by all patients for time intervals between first visit and referral, and the time interval between referral and specialist visit. Actual referrals to specialist visit time intervals were available for 69 patients. Patients had a median of 20 days and a mean of 28.7 days between referral to first visit at a specialist. For patients for which data were available who had also self-reported time between referral to first visit (n = 54), 50% reported their actual time interval correctly to within 2 weeks, 27.8% had overestimated their actual time interval by at least 2 weeks and 22.2% had underestimated their actual time interval by at least 2 weeks. 399
K Allen and CS Farah Table 2. Questionnaire results
Table 3. Anxiety about checks
Dental attendance related questions
Yes n
Do you see a dentist for regular 6 monthly check ups? Do you see a dentist when something needs fixing? Do you see the same dentist?
60
70.6%
-
-
25
29.4%
83
97.6%
-
-
2
2.4%
69
81.2%
-
-
16
18.8%
Lesion related questions
Yes n
Did you know about your lesion before screening? Did you feel it would get better with time? Did you feel it was normal? Did you feel it could be sinister? Have you experienced something similar in the past? Did you tell loved ones? Did you use products?
45
52.9%
-
-
40
47.1%
47
55.3%
1
1.2%
37
43.5%
18
21.2%
1
1.2%
66
77.6%
52
61.2%
0
0.0%
33
38.8%
16
18.8%
-
-
69
81.2%
Referral related questions
Yes n
Was it made clear why you were referred? Did you agree with your referral? Did you delay in using your referral?
84
98.8%
-
-
1
1.2%
83
97.6%
-
-
2
2.4%
6
7.1%
-
-
79
92.9%
Oral cancer related questions
Yes n
Have you heard of anyone who has had oral cancer? Should dentists be checking for oral cancer? Should doctors be checking for oral cancer? Is it beneficial for pamphlets? Beneficial for dentists to explain Beneficial for doctors to explain?
78
91.8%
-
-
7
8.2%
84
98.8%
-
-
1
1.2%
69
82.1%
-
-
15
17.9%
83
97.6%
-
-
2
2.4%
81
95.3%
-
-
4
4.7%
78
91.8%
-
-
7
8.2%
400
Unsure n
No n
Unsure n
How do you feel about checks?
n
%
Not anxious Slightly anxious Fairly anxious Very anxious Extremely anxious
49 14 15 4 3
57.6 16.5 17.6 4.7 3.5
Table 4. Patient reported time between appointments for mucosal pathology Time between discovery of lesion and seeking help n = 35* (%)
No n
Less than 2 weeks 2–4 weeks 1–3 months More than 3 months
Time between Time between first appointment referral being with health issued and first care provider appointment with and referral specialist being issued n = 74 (%) n = 74 (%)
12 (34.3%)
60 (81.1%)
35 (47.3%)
5 (14.3%) 8 (22.9%) 10 (28.6%)
3 (4.1%) 4 (5.4%) 7 (9.5%)
17 (23.0%) 17 (23.0%) 5 (6.8%)
*Only self-aware participants were included.
DISCUSSION 60
70.6%
-
-
25
29.4%
19
22.6%
-
-
65
77.4%
Unsure n
No n
Unsure n
No n
This study sought to understand patient experiences leading up to assessment and diagnosis of suspicious oral mucosal pathology. Information collected from participants increases understanding of the barriers and triggers to help seeking for oral mucosal pathology. Understanding experiences of patients referred for assessment of oral mucosal pathology can improve referral pathways and strategies. Most participants in the current study had heard of someone who had been diagnosed with oral cancer; however, this result is artificially high when compared with studies investigating the general public’s awareness of oral cancer.12,28 The results partly reflect an increased awareness of participants about oral cancer as attendees of an oral medicine clinic. The results of this study suggest that most patients are not anxious about receiving oral mucosal screening, although there were a minority of patients who reported anxiety. Of those who were anxious, worry was due to fear of finding oral cancer. The population under investigation had higher than normal awareness of oral cancer, thus they would be more aware of the devastation that a positive diagnosis would entail. It follows that there could be even less patient anxiety in the general population since oral cancer awareness is less prevalent. Further investigation into screening anxiety of the general population would be useful. Practitioners should educate patients on the relatively simple treatment of OPMD or early OSCC as opposed to late
© 2015 Australian Dental Association
Patient perspectives on oral mucosal pathology stage oral cancer. If patients understand the consequences of delaying mucosal screening, they may be motivated to seek regular examination. Studies have shown that oral mucosal screening is not always performed by dentists.29,30 Some dentists feel it is not their role to screen for mucosal pathology since they are not medical doctors. Patients will seek help where they expect that they will receive adequate care, and the results of our study suggest that most patients believe that both dentists and doctors should screen for mucosal lesions. Indeed, most patients also believed it would be beneficial for both dentists and doctors to explain what oral cancer was and how it could be caused. Most patients were aware of commonly known risk factors, such as smoking or drinking alcohol, however patients were largely unaware of the possible link between oral cancer and human papillomavirus (HPV).31 With the emergence of HPV associated oral cancer, it is of particular importance that patients are made aware of routes of HPV transmission. Educating patients on all oral cancer risk factors will enable them to assess their own oral cancer risk profile. While population based screening is not currently justified due to the relatively low prevalence of oral cancer, opportunistic screening, or targeting of groups known to be at higher risk for oral cancer may be more cost-effective.32 Opportunistic oral mucosal screening also provides an opportunity for the clinician to engage the patient in a discussion about oral cancer and enhance patient education about this disease and OPMDs generally. Most participants reported that dentists detected their oral mucosal lesion, while a small proportion of patients reported that oral health therapists or doctors detected their oral lesion. Patients with oral mucosal pathology may present to any health care setting, hence suitable educational material on this topic should be aimed at all primary HCPs. Many patients with symptomatic oral cancer will initially seek help with a doctor.33 Additionally, many patients who are at risk of oral cancer may not be regular dental attendees.34 This has implications for screening and referral protocols. Some dentists and doctors do not feel adequately trained to deal with oral mucosal pathology.30 Patients in this study expected that both dentists and doctors should check for and be able to explain oral mucosal pathology. The general public might expect similar standards of care. Adequate training for both dentists and doctors is required to meet patient expectations in this area. Most patients surveyed in this study were satisfied with the advice provided by their referring practitioner and most agreed to act on their referral. A very small proportion felt that they delayed their specialist appointment. Actual time and reported © 2015 Australian Dental Association
time between referral and first specialist visit was available for most (81.2%) patients. Actual and reported times were compared; this demonstrated that about half of patients were able to correctly record to within 2 weeks the actual time frame. Therefore, reliability of reported time frames by patients is questionable since about half were unable to report correctly the time frame and about a fifth did not record any time frame at all. Considering the median time between initial referral and survey completion of about 4.5 years, patients may be unable to accurately report time intervals due to recall bias. The median time of 20 days between referral and specialist visit shows that most patients will promptly visit a specialist when referred. The need for referring practitioners to communicate urgency to their patients when issuing a referral for oral mucosal pathology is to account for the minority of patients who delay in using their referral. Referring practitioners might also consider following up with patients subsequent to issuing a referral to ensure that patients are attending specialist appointments without delay. For cases that are highly suspicious for malignancy, practitioners should liaise with the specialist to ensure that the patient does not experience any undue delay due to difficulties securing an appointment. How a patient felt about their mucosal pathology did not have any correlation with the time taken between referral and first specialist visit. Perception of a serious condition that would not improve with time was also not correlated with whether a patient was diagnosed with OSCC or another oral mucosal lesion. Most participants perceived their condition as serious, since they felt that their lesion was not normal and that it could be something sinister. Those patients who did not feel that their condition was serious, or that their condition would get better with time were just as likely to promptly visit a specialist regarding their mucosal pathology. These results do not support the hypothesis that patients may delay affecting a referral if they do not believe that their condition is serious.35,36 This study was unable to identify a particular trait which could delay patient attendance to a specialist. This again emphasizes the importance of patient follow-up, as there may not be a particular referral communication strategy that will promote prompt use of a specialist referral. Patients in this study were generally satisfied with the advice that was given on referral, although what particular advice was provided was not investigated. Reasons for patient satisfaction with referrals would be useful to include in future studies, especially since in another study, a large proportion of patients were not happy with advice received upon their first medical consultation.3 The practitioner should be able to 401
K Allen and CS Farah gauge the patient’s emotional and social well-being to deliver medical information that the patient is able to comprehend.37 About half of the participants knew about their oral mucosal pathology prior to referral. This highlights the importance of clinicians visually examining the oral mucosa for abnormalities, since patients will not always present complaining of mucosal pathology. Even for those who were self-aware, some had lesions that were incidentally discovered by HCPs at appointments that were scheduled for other reasons (dental check-up or dental emergency). Most patients recalled ‘feeling’ something different and a smaller proportion remembered ‘seeing’ something different in their mouths. Presence of pain, seeking advice from a HCP, and seeking an explanation for the presence of oral symptoms were the most common reasons for seeking help in this study. Therefore, HCPs should enquire about changes noted by the patient relating to oral soft tissues. Most participants reported that loved ones had promoted help seeking, however a small proportion of participants recalled that loved ones advised them not to worry, or that their pathology was ‘just an ulcer’. Given that an ulcer is a common initial presentation that is remembered by oral cancer patients, greater public awareness about the significance of a nonhealing ulcer is required.3 The public know very little about the clinical presentation of oral cancer.38 Community awareness campaigns should focus attention of patients on seeking advice from a dentist if there are any changes in the appearance or sensation of their oral cavity. Patients are generally accepting of advice from HCPs. Promoting effective training among clinicians through continuing professional education will ensure that appropriate advice or referral is provided to patients, and delay is minimized. Practitioners who are not confident in their abilities might use telemedicine or electronic facilities to liaise with an oral medicine specialist for an opinion on the nature of the lesion and the need for referral. This study involved a group of patients who were referred to a private oral medicine specialist and may not capture the opinions of all individuals who have been referred for oral mucosal pathology. There are numerous referral pathways for patients with OSCC and OPMDs, including to an oral maxillofacial surgeon or an oral surgeon in either the private or public system. Future research to include these patients would be valuable to provide a better understanding on the issues that may impact on early detection of oral cancer. The small sample size, particularly of patients diagnosed with OSCC, means that these results are not generalizable. All due care was taken to ensure the self-reported questionnaire provided valid and reliable results, with data that was not considered reliable being removed. 402
CONCLUSIONS Most patient mediated delay occurred between selfdetection of a lesion and presentation to a primary HCP. Targeting this aspect of delay relies on raising community awareness about oral cancer. Many patients sought advice from loved ones prior to seeking help with a HCP and although most loved ones advised patients to seek help, there was still a small proportion who advised against it. Help seeking was delayed in these cases due to the belief that symptoms were normal. Considering that ulceration is a common presentation of OSCC, public perception that ulceration is normal may contribute to patient delay. Concern that oral mucosal screening creates patient anxiety was unfounded in this study, since most patients who were referred for suspicious oral mucosal pathology were amenable to being screened for oral mucosal pathology. Patients actually had an expectation that health professionals would perform mucosal screening and also explain what oral cancer is and how it is caused. Most patients interpreted their symptoms as something minor, even after being referred for suspicious pathology. Clinicians may be avoiding terminology that they believe will unnerve patients, as most patients were unaware of the potential significance of mucosal pathology. Clinicians should feel confident in discussing the presence of a suspicious lesion with their patients, since most patients were accepting of advice given by a HCP. AUTHORS’ CONTRIBUTIONS KA and CSF participated in study conception, design and data collection. KA performed the statistical analysis and drafted the manuscript. CSF checked results and edited the manuscript. The authors declare that they have no competing interests. ACKNOWLEDGEMENTS We thank the patients who participated in this study, the staff at the UQCCR (Fatima Dost and Lisa Dingwall) for assistance with questionnaire distribution and collection, and Dr Pauline Ford for assistance with questionnaire design. REFERENCES 1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010;127:2893–2917. 2. van der Waal I, de Bree R, Brakenhoff R, Coebergh JW. Early diagnosis in primary oral cancer: is it possible? Med Oral Patol Oral Cir Bucal 2011;16:e300–305. 3. Rogers SN, Vedpathak SV, Lowe D. Reasons for delayed presentation in oral and oropharyngeal cancer: the patients perspective. Br J Oral Maxillofac Surg 2011;49:349–353. © 2015 Australian Dental Association
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24. Allen K, Ford P, Farah C. Oral mucosal screening and referral attitudes of Australian oral health therapists and dental hygienists in Queensland. Int J Dent Hyg 2015;13:206–212. doi: 10.1111/idh.12103. 25. Allen K, Farah CS. Dental prosthetist experience with oral mucosal screening and referral. Quintessence Int 2014;45:891–897. 26. Allen K, Farah C. Screening and referral of oral mucosal pathology: a check-up of Australian dentists. Aust Dent J 2015; 60:52–58. 27. Farah CS, Ford PJ, Allen K, Vu AN, McCullough MJ. Oral cancer and potentially cancerous lesions – early detection and diagnosis. In: KUE Ogbureke, ed. Oral Cancer. ISBN: 978-95351-0228-1, InTech, doi:10.5772/30997. 28. Awojobi O, Scott SE, Newton T. Patients’ perceptions of oral cancer screening in dental practice: a cross-sectional study. BMC Oral Health 2012;12:55. 29. Klosa K, Wiltfang J, Wenz HJ, Koller M, Hertrampf K. Dentists’ opinions and practices in oral cancer prevention and early detection in Northern Germany. Eur J Cancer Prevent 2011;20:313–319. 30. Brocklehurst PR, Baker SR, Speight PM. A qualitative study examining the experience of primary care dentists in the detection and management of potentially malignant lesions. 1. Factors influencing detection and the decision to refer. Br Dent J 2010;208:E3; discussion 72-73. 31. Milbury K, Rosenthal DI, El-Naggar A, Badr H. An exploratory study of the informational and psychosocial needs of patients with human papillomavirus-associated oropharyngeal cancer. Oral Oncol 2013;49:1067–1071. 32. Speight PM, Palmer S, Moles DR, et al. The cost-effectiveness of screening for oral cancer in primary care. Health Technol Assess 2006;10:1–144, iii-iv. 33. Jovanovic A, Kostense PJ, Schulten EA, Snow GB, van der Waal I. Delay in diagnosis of oral squamous cell carcinoma; a report from The Netherlands. Eur J Cancer B Oral Oncol 1992;28B:37–38. 34. Frydrych AM, Slack-Smith LM. Dental attendance of oral and oropharyngeal cancer patients in a public hospital in Western Australia. Aust Dent J 2011;56:278–283. 35. Tromp DM, Brouha XD, Hordijk GJ, Winnubst JA, de Leeuw JR. Patient factors associated with delay in primary care among patients with head and neck carcinoma: a case-series analysis. Fam Prac 2005;22:554–559. 36. Morse DE, Velez Vega CM, Psoter WJ, et al. Perspectives of San Juan healthcare practitioners on the detection deficit in oral premalignant and early cancers in Puerto Rico: a qualitative research study. BMC Public Health 2011;11:391. 37. Newton JT. Reactions to cancer: communicating with patients, family and carers. Oral Oncol 2010;46:442–444. 38. Hertrampf K, Wenz HJ, Koller M, Wiltfang J. Public awareness about prevention and early detection of oral cancer: a population-based study in Northern Germany. J Craniomaxillofac Surg 2012;40:e82–86.
Address for correspondence: Professor Camile S Farah The Australian Centre for Oral Oncology Research and Education (ACORE) PO Box 88 RBWH Herston QLD 4029 Email: [email protected]
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