Oral Oncology 50 (2014) 956–962
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Oral Oncology journal homepage: www.elsevier.com/locate/oraloncology
Review
A systematic review of patient acceptance of screening for oral cancer outside of dental care settings Priyamvada Paudyal, Francesca D. Flohr, Carrie D. Llewellyn ⇑ Division of Public Health & Primary Care, Brighton and Sussex Medical School, Brighton BN1 9PH, UK
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Article history: Received 26 March 2014 Received in revised form 16 June 2014 Accepted 20 July 2014 Available online 7 August 2014 Keywords: Oral Cancer Screening Acceptance Satisfaction Knowledge
s u m m a r y This systematic review summarised the literature on patient acceptability of screening for oral cancer outside dental care settings. A comprehensive search of relevant literature was performed in EMBASE, MEDLINE, Cochrane Database of Systematic Reviews, CINAHAL, psycINFO, CANCERLIT and BNI to identify relevant articles published between 1975 and Dec 2013. Studies reporting acceptability of oral cancer screening to undiagnosed individuals attending non-dental settings were eligible for inclusion. A total of 2935 references were initially identified from the computerised search but 2217 were excluded after screening the titles. From the abstracts of the remaining 178 articles, 47 full text articles were retrieved for further scrutiny, and 12 studies were found to be eligible for inclusion. In these studies, knowledge about oral cancer, anxiety related to the screening process, preference for care provision, and financial cost were influencing factors for the acceptance of screening. Written information provided to patients in primary care was reported to boost immediate knowledge levels of oral cancer, lessen anxiety, and increase intentions for screening. The majority of screening methods were entirely acceptable to patients; lack of acceptability from the patients’ viewpoint was not a significant barrier to carrying out opportunistic screening of high-risk populations. In conclusion, the available evidence suggests that acceptance of, and satisfaction with oral cancer screening is high, particularly where patients have previously been educated about oral cancer. Further research focusing on patient’s preferences would enable streamlining of the approach to oral cancer screening taken by any national programme. Ó 2014 Elsevier Ltd. All rights reserved.
Introduction The incidence rate of oral cancer in the UK has risen by a third in the last decade with 6539 new cases diagnosed in 2010 [1]. Despite advances in surgical and management techniques, the overall 5year survival rate for oral cancer has remained static (at 50%) in the past few decades [2]. Preventing late-stage oral cancer by increasing awareness among the population and thus encouraging earlier presentation, or secondary prevention by screening and early detection, are the most effective means of reducing the burden of oral cancer [3]. However, studies have reported that approximately 30% of patients delay seeking help for more than 3 months following the self-discovery of symptoms of oral cancer [4] and 40% of patients with oral cancer present with advanced disease (stages III and IV) [5]. Delay in presentation (patient delay) and diagnosis (professional delay) has been linked with poorer disease ⇑ Corresponding author. Address: Room 317, Mayfield House, Brighton & Sussex Medical School, Brighton BN1 9PH, UK. Tel.: +44 (0) 1273 642187; fax: +44 (0) 1273 644440. E-mail address: [email protected] (C.D. Llewellyn). http://dx.doi.org/10.1016/j.oraloncology.2014.07.007 1368-8375/Ó 2014 Elsevier Ltd. All rights reserved.
prognosis [6,7] and worse health related quality of life outcomes [8], incurring additional financial and physical cost to both the healthcare system and the patients. Screening programmes for some major cancers, such as colorectal cancer and cervical cancer have been proven effective in facilitating earlier detection and thus, improving mortality rates and decreasing the incidence of these cancers [9,10]. However, screening for other cancers such as breast cancer, has remained controversial as the evidence shows that benefit from attending screening is ten times smaller than the risk associated with overdiagnosis and unnecessary treatment [11]. The only national screening programme for oral cancers is in Cuba [12]. Developed countries have not yet implemented population-based screening programs for oral cancers, although it has been advocated that opportunistic screening should be carried out as part of a periodic health examination [13,14]. At present, there is no national screening programme for oral cancer in the UK. A study was conducted to determine the feasibility of invitational screening programme for oral cancer in the UK [15]. A total of 4348 registered patients, aged 40 years and over were invited for screening by post. Only 23% (n = 958) accepted the screening, only twelve were referred with
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suspicious lesions and only eight attended the referral appointment. The study suggested that a population based screening programme for oral cancer may not be effective in reducing morbidity and mortality, and the establishment of such a programme may not be cost-effective. In 2010, Speight and Warnakulasuriya produced a valuable report that evaluated the evidence for the implementation of screening for oral cancer in the UK against the National Screening Committee (NSC) criteria [16]. The report suggested that there is still considerable uncertainty around the natural history of the disease and thus, a UK national screening programme cannot be advocated. The review by Warnakulasuriya and Cain [17] also highlighted the need of further research in several specific and key areas to justify the establishment of a nationwide screening programme. The review suggested that more research is required to identify early disease markers to understand the disease progression and to find the best test available for the earlier detection of the disease. The necessity of additional studies in primary care settings to define the values of already existing tests, and the identification of the most sensitive and specific test on offer were also emphasised in the review. Evidence from the recently updated Cochrane review on oral visual examination (OVE) as a part of a population based screening program for oral cancer reported improved survival and a significant stage shift to diagnosis of early stage disease across the population as a whole, and a 24% reduction in mortality in high-risk groups (males who used tobacco and/or alcohol) [18]. However, the findings of the review were based on one randomised trial conducted in a high prevalence population in Kerala, India, so its generalisability to a Western population is uncertain. In the UK, General Dental Practitioners (GDPs) currently hold the main responsibility for the early detection of oral cancer [19]. It appears likely that GDPs should detect more cases of oral cancer opportunistically than General Medical Practitioners (GPs) because GDPs’ examine the oral cavity regularly. However, it has been reported that where patients do present with symptoms, only 40% of such presentations are to the GDPs [20]. In a widespread GP Patient Survey conducted between July to September 2013 in the UK, 1.3 million adults were asked about access to NHS dentistry. A total of 450,000 adults replied, of whom only 57% visited for dental check-ups in the previous two years [21]. As high-risk individuals (those who smoke tobacco, regularly drink alcohol and are over 45 years old) comprise the least likely cohort to be regular attendees for dental check-ups [22,23], opportunistic screening for oral cancer, if focused only on the dental examination, may miss a large proportion of this high-risk population [24]. As these high-risk individuals are more likely to visit general medical physicians than dentists, primary care may provide the opportunity for detection of potential cases of oral cancer. Evidence to date also concurs that the most cost-effective method of screening would be opportunistic programmes targeting high-risk individuals attending primary care [3]. For any screening programme to be established, it is essential that the programme should be acceptable to the patient and the benefits of the screening programme must outweigh the physical and psychological harm to the patient such that the patient is willing to engage with the programme. There has been a plethora of research on patient delay on oral cancer [7,25] and cost effectiveness of a UK wide oral cancer screening programme [3]. However, there is a paucity of studies looking at patients’ preferences, satisfaction and willingness to undergo oral cancer screening, especially in non-dental care settings. Patient’s preferences and perspectives are important in successful tailoring of screening services. This systematic review aims to determine the acceptability of screening for oral cancer outside of dental care settings. We believe that the synthesis will contribute to the evidence in determining the feasibility of an opportunistic screening programme in the UK.
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Materials and methods Eligibility criteria Studies were eligible if they (i) reported acceptability of oral cancer screening to undiagnosed individuals (ii) included primary data; (iii) were published in English. Studies were excluded if they only focused on healthcare professionals’ attitudes towards screening of oral cancer, referred to malignancies outside the oral cavity and screening for cancer in general, focused mainly on patients’ acceptability of diagnosis of oral cancer as opposed to detection, and/or compliance with specialist care, and those that were carried out in dental settings. Information sources and search We searched EMBASE, MEDLINE, Cochrane Database of Systematic Reviews, CINAHAL, psycINFO, CANCERLIT and BNI to identify relevant articles published between 1975 and Dec 2013. References in each of the identified articles were further screened for relevant references. Three comprehensive search themes were used while conducting the search in the electronic databases: (ii) identification of the relevant disease of interest, i.e. oral cancer, and (ii) identification of the relevant terms for screening and (iii) identifying the relevant terms related to acceptability and satisfaction. We then combined the results of the searches using the Boolean operator AND (Fig. 1). Study selection and data extraction Two reviewers (PP and FF) independently carried out the search, screened the titles of the articles and removed any irrelevant and duplicate articles. Abstracts of the remaining articles were assessed applying the inclusion criteria. Any disagreements in selections were discussed and resolved during consensus meetings involving a third investigator (CL). Relevant studies are presented in Fig. 2. We extracted the relevant information from the selected studies: study ID, study aim, sample characteristics, study design and number of participants, data collection method and period and key factors indicating screening acceptability to patients. The results are summarised in Table 1. Results A total of 2935 references were initially identified from the computerised search but 2217 were excluded after screening the titles. From the abstracts of the remaining 178 articles, 47 full text articles were retrieved for further scrutiny, and 12 studies were found to be eligible for inclusion. The study design varied across the studies; five were cross sectional [26–30], three were randomised controlled trials (RCTs) [31–33], three were focus group and/or interviews [34–36], and one pre-post design [37]. The majority of the studies (n = 7) were conducted in the UK [28,30–34,36], two in the USA [35,37], one in Canada [29] and two in India [26,27]. The details of the included studies are provided in Table 1. Factors associated with the acceptability of oral cancer screening Preference for care provision Three studies evaluated patients’ preferences for care provision for oral cancer screening [34–36]. In all three studies, participants stated their preference for having primary care physicians perform the oral cancer examination. General practice was seen as an appropriate setting for screening due to its local nature, ease of
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Fig. 1. Terms used to search the electronic databases.
access, familiarity and relevance for a health-related intervention [34,36]. Participants stated their preference for receiving information about oral cancer through personal interaction with their primary care practitioners [34]. Lack of trust towards dentists was stated as a barrier in one study where participants perceived a dentist as a ‘tooth specialist’, rather than a ‘mouth specialist’, who lacked the power of a doctor to make referrals and write prescriptions [34]. Cost and related factors Financial cost was perceived as an influencing factor for the acceptance of screening. In Dodd et al. [35], willingness to accept a free oral cancer examination was high among males (100%; n = 32) whereas younger females did not uniformly agree with the idea. The females in the study stated that they would decline the opportunity to be screened even if screening was conducted at their worksite and offered free. Participants in another focus group study also perceived that the screening should be cost free and speedy [34]. However, there were stark differences in participants’ characteristics, cultural beliefs regarding oral cancer, and health care provision across these two studies conducted in different countries, which may have affected participants’ opinion about the financial cost related to screening.
Knowledge and awareness of oral cancer It was frequently reported that patients had inadequate knowledge about signs and symptoms of oral cancer [34–37] and a lack of awareness of the importance of a recommendation for oral cancer screening [34,35]. In one study conducted amongst a high-risk population in Canada, 88% of the participants were unaware of the disease [37]. However, in a study from India, the overall awareness of oral cancer of study participants was over 80% following health education using the Mouth Self Examination (MSE) brochure, leading to 95% of participants correctly identifying the different risk factors [26]. The need for more public information about oral cancer was also reported in some studies [35,36]. Interventions such as written information materials provided to patients in primary care were reported to have the potential to boost immediate knowledge levels of oral cancer, thus resulting in increased intentions towards oral cancer screening [32,33]. Anxiety related to symptom and screening procedure Patients perceived that knowing more about oral cancer may make them more anxious should they notice any disease symptom [36]. However, studies aimed at increasing knowledge and awareness of oral cancer reported that access to information does not increase pre-procedural fear and anxiety of participants [31–33].
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Databases searched
2935 studies identified
Screening of titles and abstracts for relevant studies
47 relevant studies identified
Studies read in full and application of inclusion criteria
12 studies selected for inclusion for review.
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Impact of intervention on compliance of screening In one study conducted among a high-risk population in India [26], compliance with instructions to perform MSE following access to an information leaflet was high, with 87% of the participants practising MSE and 95% believing that early detection could improve the chances of cure. Whilst the sensitivity of MSE was very low at 18%, the specificity was high at 99.9% (PPV = 72%, NPV = 99%). In another study, participants underwent an oral examination by their dentist and then performed MSE after reading an instructive leaflet [28]. The study found that half of the participants (51%) correctly diagnosed the symptoms and the majority (74%) of participants found MSE easy to perform. However, the sensitivity and specificity of MSE was 33% (95% CI 11–65%) and 17% (95% CI, 6–40%) respectively. Perceived benefits of and barriers to oral cancer exam Patients perceived that screening would be helpful to detect disease early, and would lead to longer life, peace of mind, prevention and awareness [35,36]. Lack of awareness of oral cancer, the belief that oral cancer is rare, uncertainty of the exam process, fear of pain, and costs related to oral cancer exam were cited as the major barriers to the oral cancer exam in a focus group study conducted by Dodd et al. [35]. Individuals in this study suggested that there is a need for convenient locations, extended hours in health clinics, mobile clinics, Saturday hours and also a desire for low to no-cost dental examinations. Lack of confidence in performing MSE was stated as another barrier [28].
Fig. 2. Article selection process.
One study reported that information leaflets did not change concerns regarding MSE, although one-to-one interaction sessions were helpful in reducing MSE related anxiety [31]. Similar results were reported in other studies where anxiety associated with the screening was not influenced by leaflet access [33], or were reduced [32]. One study reported pre-procedural anxiety in one third of participants (31%), however, on completion of the screening, there was almost unanimous agreement that the procedure was painless [30].
Socio-demographic characteristics Across the studies, there were no clear relationships between socio-demographic factors and acceptance of screening. The studies were extremely varied culturally and ethnically.
Impact of written information on intention to accept oral cancer screening Two RCTs assessed the influence of Patient Information Leaflets (PIL) on intentions to accept screening (32, 33). Both studies found a positive influence of information leaflets; those receiving a leaflet were more likely to accept an oral cancer screen if offered. The leaflet group also had stronger beliefs that health personnel and family would expect them to accept screening and perceived that screening would be less of a waste of time and not painful [33]. The third RCT assessed the impact of a leaflet and a one-to-one interaction on earlier presentation of oral cancer, including MSE [31]. The study reported that the interventions resulted in an increased knowledge of oral cancer, increased perceived confidence to seek help and perform MSE, and reduced anticipated delay in seeking help for potentially malignant oral symptoms. Rwamugira and Maree [37] found that the quality of the written material affected the individuals’ decision to uptake screening; individuals who found the information easy to understand were more likely to be motivated to take up screening.
Patient experiences and acceptance of specific screening activities The acceptance of oral visual examinations (OVE) conducted in community screening programmes varied across studies. In a study conducted among tobacco users in India, overall acceptance and satisfaction levels of OVE in a mobile setting were encouraging, with 98% of the participants feeling comfortable with oral screening tests [27]. Similarly another study in Canada also reported high acceptance of OVE (98%) among high-risk individuals (based on risk factors, lack of access to care, and the high frequency of oral mucosal anomalies), but, acceptance of biopsy for abnormal findings and follow-up was low with only 12 out of 31 (39%) patients with clinical leukoplakia accepting the biopsy [29]. In contrast, a study from South Africa, reported poor acceptance of OVE conducted in mobile clinics with only 4.9% (out of the 1320 eligible adults in the community) accepting a screen during the 6-week period [34]. Of those who accepted the examination, only 12% were high-risk participants (specified as men older than 40 years of age). Feaver et al. [30] found that the use of Orascreen (a screen using toluidine blue dye) in aiding the screening for oral cancer was highly acceptable to patients; 100% individuals accepted the screening, 83% described screening as ‘a comfortable experience’ and 95% of the respondents expressed a willingness take part in future oral health screening. Discussion This systematic review has considered the available evidence relating to patients’ acceptability of oral cancer screening in nondental settings. Although some attempts have been made to explore patients’ attitudes and responses towards oral cancer screening processes, the acceptability of screening for oral cancer to patients does not appear to have been the specific focal point of any published studies. The overarching theme from the reviewed studies appears to be that, while the potential barriers to screening and diagnosis are diverse, the majority of methods of screening for oral cancer are entirely acceptable to patients per se. Lack of acceptability of screening from the patients’ viewpoint
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Table 1 Details of the studies included in the review in chronological order. Study
Sample characteristics
Study design (No of participants)
Key factors indicating screening acceptability to patients
Zohoori et al. [34]
Male smokers and/or drinkers, irregular dental attenders aged 40–61 years living in economically deprived area of Teesside, UK
Focus group (N = 18)
Scott et al. [31]
Smokers aged between 45 and 65 years recruited from three GP practices in South East London, UK
RCT; patients randomised to three groups, leaflets or one to one instruction or control group. Selfreporting questionnaire at 1 month post intervention (N = 112)
Kumar et al. [27]
Female smokers aged between 30 and 65, India
Interview administered questionnaire after being screened (N = 59)
Elango et al. [26]
Individual aged between 10 and 99 from two adjacent coastal villages in Kerala, India
Interview administered questionnaire at 4 weeks after patients read brochure regarding MSE (N = 34,766)
Scott et al. [36]
Smokers and/or drinkers aged between 45 and 65 years recruited from a GP practices in South East London, UK
Study 1: Semi-structured interviews N = 25 Study 2: Use of ‘think-aloud protocol’; participants read the leaflets and at the same time verbalise their thought and feelings (N = 14)
Rwamugira and Maree [37] Scott et al. [28]
Individual aged 18 and over registered as a client of a Nursing community of practice, USA
Structured interview pre- and post-2 months after nursing intervention (N = 65)
Lack of knowledge and awareness of oral cancer and its signs and symptoms. Preference to be screened by GP and family physicians during routine health checks, and preference for the use of a ‘‘health’’ setting as opposed to a ‘‘dental’’ setting for screening Brief interventions seem to be effective tool to encourage early detection of oral cancer. The intervention groups felt significantly more confident and more likely to perform MSE than the control group High level of acceptance and satisfaction with OVE mobile screening clinic; 98.31% were satisfied with the test procedure and examination room, 100% were satisfied with the privacy level MSE shown to be highly acceptable screening tool but effectiveness questionable; MSE identifies high-risk lesions well (detection of red patches 66.7% but 87% not detected case were of white patches Lack of knowledge; concern about wasting PCP’s time with minor symptoms, lack of confidence in performing MSE although participants found MSE straightforward and easy to follow. GP practice was seen as an appropriate setting for screening Screening uptake was poor (4.9%). The strategy used to improve knowledge and awareness was successful
Smokers aged over 45 recruited from GP’s list in South East London, UK
Self-report questionnaire after performing MSE (participants read information leaflet prior to MSE). Proforma (dentist) (N = 54) Focus group (N = 56)
Dodd et al. [35] Poh et al. [29]
Humphris et al. [32] Humphris and Field [33] Feaver et al. [30]
African Americans aged between 35 and 75 recruited at a private research firm, USA Individuals (mean age 47 years) attending community outreach dental clinic, Vancouver, Canada Participants (mean age 44 years) were recruited from 14 general practices in the north west of England, UK Individuals (mean age 43 years, SD 15 years) were recruited from dental and medical waiting rooms in the North West of England, UK Employees aged between 40 and 59 years in a large retail chain in the UK
Structured individual interviews prior to OVE (N = 204)
RCT; patients randomised either to leaflet or nonleaflet group, a questionnaire completed immediately post intervention (N = 800) RCT; patients randomised either to leaflet or nonleaflet group, a questionnaire completed immediately post intervention (N = 769) Self-reported questionnaire Survey (N = 140)
does not appear to be a significant barrier to carrying out opportunistic screening of high risk populations. Inadequate knowledge about oral cancer and screening processes was common and acted as an obstacle to the uptake of screening. Other barriers included financial and logistical barriers such as cost related to the screening process and transportation. Provision of information about the disease seems to improve knowledge and awareness of symptoms, and have a positive impact on likely acceptance of oral cancer screening [32,33]. Where individuals expressed some fear and anxiety with regard to screening, it was demonstrably lessened by education about the benefits of being screened for the disease. However, it is still unclear whether the effects of these brief interventions translate into significant clinical differences such as earlier diagnosis, treatment and therefore a reduction in morbidity and mortality [31]. Preference for seeking help from GPs rather than from dentists, and preference towards a general practice setting as opposed to dental clinics was stated in many studies, although this bias may reflect the exclusion criteria for the review. Previous studies have indicated that the majority of patients (over 70%) are more likely
The risk groups were poor at correctly identifying the presence or absence of potentially malignant oral lesions. The majority (74%) found MSE to be very easy or easy Lack of knowledge of risk factors and severity of late diagnosis, preference for having primary care physicians perform the oral cancer exam Acceptance of screening was high (98%); however, acceptance of biopsy for abnormal findings and follow-up was low (only 12 out of 31 patients with clinical leukoplakia were biopsied) PIL demonstrated an increase in intention to have an oral cancer screen and reduced anxiety PIL shown to be useful in improving patients’ knowledge of oral cancer and intention to accept an oral cancer screen Anxiety about oral health screen not raised by leaflet exposure Toluidine blue shown to be highly acceptable screening tool
to consult a GP should symptoms arise, and fewer than half to a dentist [38]. In addition, studies conducted in dental settings have reported low uptake (24%) of free mouth checks [39]. This suggests that oral cancer screening in a general practice settings may be more efficient and acceptable to participants. However, to prevent patients and the GP practice being overwhelmed by various interventions for each cancer type, the screening of oral cancer could feasibly be incorporated into a wider early cancer detection programme [31]. Our intention was to review the acceptability of oral cancer screening as a whole rather than specific screening methods. It appears likely that MSE would have high levels of acceptability to patients, as it is free and unlikely to induce the same anxiety as a visit to the dentist. However, MSE is subject to the same hindrances as other screening methods, namely low levels of patient awareness and questionable reliability of results. Any new screening technique or adjunct devices for use in the UK are required to conform to the National Screening Committee (NSC) criteria before being recommended for implementation. These criteria are robust and request evidence for a simple, safe, precise and validated
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screening test that is likely to be acceptable to the population [40]. Individuals were considerably more likely to conduct MSE after education about oral cancer but sensitivity and specificity of the examination were highly variable between studies [26,28]. Nevertheless, the encouragement of MSE is not without its benefits because it is likely to increase overall understanding of oral cancer and bring about earlier presentations as a result. The studies concerning a specific screening method such as Orascreen were highly acceptable to patients but provided no evidence relating to sensitivity or specificity of results [30]. Although we did not specifically look at the diagnostic accuracy of the screening methods, the sensitivity and specificity of the screening methods varied across the studies. In a recent Cochrane review on diagnostic test accuracy of conventional oral examination as a screening test in primary settings, sensitivity estimates ranged from 0.50 (95% CI 0.07–0.93) to 0.99 (95% CI 0.97–1.00) and specificity ranged between 0.98 (95%CI 0.92–1.00) and 0.99 (95% CI 0.99–0.99) [41]. Not much is known about the relationship between test performance and patient acceptability of oral cancer screening, however, high levels of sensitivity and specificity are important as there is a risk of false reassurance for those with false negative results and unnecessary anxiety for those with false-positive results [28]. The overall acceptance and satisfaction with OVE conducted in mobile settings was encouraging in a study conducted in India suggesting that similar screening programmes may be a feasible option in a resource poor setting. However, the screening uptake with OVE mobile clinics was disappointing in another study conducted in Africa indicating that barriers to screening uptake should be explored further and adapted according to the local setting. It is not known how these findings would relate to similar ethnic groups at high risk in the UK. Some variations regarding acceptance and experiences of oral cancer screening were observed according to socio-demographic profile of the participants. This highlights that interventions and strategies should be targeted closely to specific at risk groups. This systematic review is subject to a number of limitations. As there was wide variation in the design of the studies included in the review, we did not assess the quality of the individual study. In addition, studies that were not written in English were excluded. Due to the high incidence of oral cancer in the Indian Subcontinent, it may have been useful to include more literature from this region, potentially in local languages. Nevertheless, this review did include papers from the UK, the USA, South Africa and India. Cultural differences between these countries are likely to have a major effect on both incidence rates and patient attitudes but it has not been possible to explore these differences in detail. In addition, studies that did not focus on oral cancer (as opposed to other cancers) were excluded. Relevant information from studies examining cancer screening in general may therefore have been overlooked. The small sample sizes used in some studies make it difficult to reliably apply the findings to the general population. However, each study acknowledged this limitation. Due to the relatively low incidence of oral cancer in the UK, this limitation appears somewhat unavoidable, particularly in studies where the selection criteria include younger patients. In addition, this review only explored the views of patients who accepted screening. Future studies need to explore reasons for non-uptake of screening which may be helpful to inform interventions to address potential barriers for screening and formulate strategies to facilitate earlier diagnosis of oral cancer, which are acceptable to patients. In summary, the available evidence suggests that acceptance of, and satisfaction with oral cancer screening is high, particularly where patients have previously been educated about oral cancer. This indicates that existing screening methods are generally acceptable, and where they at first appear not to be, the explanation may be a lack of understanding of the screening process rather
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than a lack of acceptability of the process. Further research focusing on patient’s preferences would enable streamlining of the approach to oral cancer screening taken by any national programme. Conflict of interest statement None declared. References [1] Cancer Research UK. Oral cancer Key Facts. [Accessed on 10.12.13]. [2] Warnakulasuriya S. Causes of oral cancer – an appraisal of controversies. Brit Dent J 2009;207:471–5. [3] Speight PM, Palmer S, Moles DR, Downer MC, Smith DH, Henriksson M, et al. The cost-effectiveness of screening for oral cancer in primary care. HTA 2006;10(14). [4] Allison P, Locker D, Feine JS. The role of diagnostic delays in the prognosis of oral cancer: a review of the literature. Oral Oncol 1998;34:161–70. [5] Rogers SN, Vedpathak SN, Lowe D. Reasons for delayed presentation in oral and oropharyngeal cancer: the patients perspective. Brit J Oral Max Surg 2011;49:349–53. [6] Kowalski LP, Carvalho AL. Influence of time delay and clinical upstaging in the prognosis of head and neck cancer. Oral Oncol 2001;37:94–8. [7] Rogers SN, Brown JS, Woolgar JA, Lowe D, Magennis P, Shaw RJ, et al. Survival following primary surgery for oral cancer. Oral Oncol 2009;45:201–11. [8] Rogers SN, Lowe D, Fisher SE, Brown JS, Vaughan ED. Health related quality of life and clinical function in patients treated by primary surgery for oral cancer. Brit J Oral Max Surg 2002;40:11–8. [9] Hewitson P, Glasziou P, Watson E, Towler B, Irwig L. Cochrane systematic review of colorectal cancer screening using the fecal occult blood test (hemoccult): an update. Am J Gastroenterol 2008;103:1541–9. [10] Peirson L, Fitzpatrick-Lewis D, Ciliska D, Warren R. Screening for cervical cancer: a systematic review and meta-analysis. Syst Rev 2013;2:35. [11] Gøtzsche PC, Jørgensen KJ. Screening for breast cancer with mammography. Cochrane Database Syst Rev 2013. Art. No.: CD001877. http://dx.doi.org/ 10.1002/14651858.CD001877.pub5. [12] Frenandez GL, Sankaranarayanan R, Lence AJJ, Rodriguez SA, Maxwell PD. An evaluation of the oral cancer control program in Cuba. Epidemiology 1995;6:428–31. [13] Smith RA, Cokkinides V, Brooks D, et al. Cancer screening in the United States, 2011: a review of current American Cancer Society guidelines and issues in cancer screening. CA Cancer J Clin 2011;61:8–30. [14] Bedi R, Butterwort M, Craig G, Langdon J, Lowndes P, Nolan A. Opportunistic oral cancer screening: a management strategy for dental practice. BDA News 2000;6:1–34. [15] Jullien JA, Zakrzewska JM, Downer MC, Speight PM. Attendance and compliance at an oral cancer screening programme in a general medical practice. Eur J Cancer B Oral Oncol 1995;31:202–6. [16] Speight PM, Warnakulasuriya S. Evaluation of screening for oral cancer against NSC Criteria; 2010. [Accessed on 05.01.13]. [17] Warnakulasuriya S, Cain N. Screening for oral cancer: contributing to the debate. J Investig Clin Dent 2011;2:2–9. [18] Brocklehurst P, Kujan O, O’Malley LA, Ogden G, Shepherd S, Glenny AM. Screening programmes for the early detection and prevention of oral cancer. Cochrane Database Syst Rev 2013(11). http://dx.doi.org/10.1002/ 14651858.CD004150.pub. Art. No.: CD004150. [19] McGurk M, Scott SE. The reality of identifying early oral cancer in the general dental practice. Br Dent J 2010;208:347–51. [20] Hollows P, McAndrew PG, Perini MG. Delays in the referral and treatment of oral squamous cell carcinoma. Br Dent J 2000;188:262–5. [21] GP Patient Survey Dental Statistics; July to September 2013, England. [Accessed on 18.12.13]. [22] Netuveli G, Sheiham A, Watt RG. Does the ‘inverse screening law’ apply to oral cancer screening and regular dental check-ups? J Med Screen 2006;13:47–50. [23] Williams M, Scott S. Is there scope for providing oral cancer health advice in dental access centres? Br Dent J 2008;205:1–3, E16. [24] Macpherson LM, McCann MF, Gibson J, Binnie VI, Stephen KW. The role of primary healthcare professionals in oral cancer prevention and detection. Br Dent J 2003;195:277–81. [25] Scott SE, Grunfeld EA, Main J, McGurk M. Patient delay in oral cancer: a qualitative study of patients’ experiences. Psycho-Oncology 2006;15:474–85. [26] Elango KJ, Anandkrishnan N, Suresh A, Iyer SK, Ramaiyer SK, Kuriakose MA. Mouth self-examination to improve oral cancer awareness and early detection in a high-risk population. Oral Oncol 2011;47:620–4. [27] Kumar Y, Mishra G, Gupta S, Shastri S. Cancer screening for women living in urban slums-acceptance and satisfaction. Asian Pacific J Cancer Prev 2011;12:1681–5. [28] Scott SE, Rizvi K, Grunfeld EA, McGurk M. Pilot study to estimate the accuracy of mouth self-examination in an at-risk group. Head Neck 2010;32:1393–401.
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[29] Poh CF, Hislop G, Currie B, Lee R, Sikorski S, Zed C, et al. Oral cancer screening in a high-risk underserved community: Vancouver Downtown Eastside. J Health Care Poor Undeserved 2007;8:767–78. [30] Feaver GP, Morrison T, Humphris G. A study to determine the acceptability in patients and dentists of toluidine blue in screening for oral cancer. Primary Dent Care 1999;6:45–50. [31] Scott SE, Khwaja M, Low EL, Weinman J, Grunfeld EA. A randomised controlled trial of a pilot intervention to encourage early presentation of oral cancer in high risk groups. Patient Educ Couns 2012;88:241–8. [32] Humphris GM, Ireland RS, Field EA. Randomised trial of the psychological effect of information about oral cancer in primary care settings. Oral Oncol 2001;37:548–52. [33] Humphris GM, Field EA. The immediate effect on knowledge, attitudes and intentions in primary care attenders of a patient information leaflet: a randomized control trial replication and extension. Brit Dent J 2003;194:683–8. [34] Zohoori FV, Shah K, Mason J, Shucksmith J. Identifying factors to improve oral cancer screening uptake: a qualitative study. PLoS ONE 2012;7:e47410. [35] Dodd VJ, Watson JM, Choi Y, Tomar SL, Logan HL. Oral cancer in African Americans: addressing health disparities. Am J Health Behav 2008;32:684–92.
[36] Scott SE, Weinman J, Grunfeld EA. Developing ways to encourage early detection and presentation of oral cancer: what do high-risk individuals think? Psychol Health 2011;26:1392–405. [37] Rwamugira J, Maree JE. The findings of a nurse-lead intervention for detection and prevention of oral cancer. A pilot study. EurJ Cancer Care 2012;21:266–73. [38] Eadie D, MacKintosh AM, MacAskill S, Brown A. Development and evaluation of an early detection intervention for mouth cancer using a mass media approach. Br. J Cancer 2009;101:S73–9. [39] Lowry RJ, Archer A, Howe D. Mouth Cancer: North East pilot evaluation report Oral Cancer Case-finding Intervention Project (OCCIP). [Accessed on 21.01.13]. [40] National Screening committee. Criteria for appraising the viability, effectiveness and appropriateness of a screening programme. [Accessed on 25.02.13]. [41] Walsh T, Liu JLY, Brocklehurst P, Glenny AM, Lingen M, Kerr AR, et al. Clinical assessment to screen for the detection of oral cavity cancer and potentially malignant disorders in apparently healthy adults. Cochrane Database Syst Rev 2013. http://dx.doi.org/10.1002/14651858.CD010173.pub. Art. No.: CD010173.
Contents lists available at ScienceDirect
Oral Oncology journal homepage: www.elsevier.com/locate/oraloncology
Review
A systematic review of patient acceptance of screening for oral cancer outside of dental care settings Priyamvada Paudyal, Francesca D. Flohr, Carrie D. Llewellyn ⇑ Division of Public Health & Primary Care, Brighton and Sussex Medical School, Brighton BN1 9PH, UK
a r t i c l e
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Article history: Received 26 March 2014 Received in revised form 16 June 2014 Accepted 20 July 2014 Available online 7 August 2014 Keywords: Oral Cancer Screening Acceptance Satisfaction Knowledge
s u m m a r y This systematic review summarised the literature on patient acceptability of screening for oral cancer outside dental care settings. A comprehensive search of relevant literature was performed in EMBASE, MEDLINE, Cochrane Database of Systematic Reviews, CINAHAL, psycINFO, CANCERLIT and BNI to identify relevant articles published between 1975 and Dec 2013. Studies reporting acceptability of oral cancer screening to undiagnosed individuals attending non-dental settings were eligible for inclusion. A total of 2935 references were initially identified from the computerised search but 2217 were excluded after screening the titles. From the abstracts of the remaining 178 articles, 47 full text articles were retrieved for further scrutiny, and 12 studies were found to be eligible for inclusion. In these studies, knowledge about oral cancer, anxiety related to the screening process, preference for care provision, and financial cost were influencing factors for the acceptance of screening. Written information provided to patients in primary care was reported to boost immediate knowledge levels of oral cancer, lessen anxiety, and increase intentions for screening. The majority of screening methods were entirely acceptable to patients; lack of acceptability from the patients’ viewpoint was not a significant barrier to carrying out opportunistic screening of high-risk populations. In conclusion, the available evidence suggests that acceptance of, and satisfaction with oral cancer screening is high, particularly where patients have previously been educated about oral cancer. Further research focusing on patient’s preferences would enable streamlining of the approach to oral cancer screening taken by any national programme. Ó 2014 Elsevier Ltd. All rights reserved.
Introduction The incidence rate of oral cancer in the UK has risen by a third in the last decade with 6539 new cases diagnosed in 2010 [1]. Despite advances in surgical and management techniques, the overall 5year survival rate for oral cancer has remained static (at 50%) in the past few decades [2]. Preventing late-stage oral cancer by increasing awareness among the population and thus encouraging earlier presentation, or secondary prevention by screening and early detection, are the most effective means of reducing the burden of oral cancer [3]. However, studies have reported that approximately 30% of patients delay seeking help for more than 3 months following the self-discovery of symptoms of oral cancer [4] and 40% of patients with oral cancer present with advanced disease (stages III and IV) [5]. Delay in presentation (patient delay) and diagnosis (professional delay) has been linked with poorer disease ⇑ Corresponding author. Address: Room 317, Mayfield House, Brighton & Sussex Medical School, Brighton BN1 9PH, UK. Tel.: +44 (0) 1273 642187; fax: +44 (0) 1273 644440. E-mail address: [email protected] (C.D. Llewellyn). http://dx.doi.org/10.1016/j.oraloncology.2014.07.007 1368-8375/Ó 2014 Elsevier Ltd. All rights reserved.
prognosis [6,7] and worse health related quality of life outcomes [8], incurring additional financial and physical cost to both the healthcare system and the patients. Screening programmes for some major cancers, such as colorectal cancer and cervical cancer have been proven effective in facilitating earlier detection and thus, improving mortality rates and decreasing the incidence of these cancers [9,10]. However, screening for other cancers such as breast cancer, has remained controversial as the evidence shows that benefit from attending screening is ten times smaller than the risk associated with overdiagnosis and unnecessary treatment [11]. The only national screening programme for oral cancers is in Cuba [12]. Developed countries have not yet implemented population-based screening programs for oral cancers, although it has been advocated that opportunistic screening should be carried out as part of a periodic health examination [13,14]. At present, there is no national screening programme for oral cancer in the UK. A study was conducted to determine the feasibility of invitational screening programme for oral cancer in the UK [15]. A total of 4348 registered patients, aged 40 years and over were invited for screening by post. Only 23% (n = 958) accepted the screening, only twelve were referred with
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suspicious lesions and only eight attended the referral appointment. The study suggested that a population based screening programme for oral cancer may not be effective in reducing morbidity and mortality, and the establishment of such a programme may not be cost-effective. In 2010, Speight and Warnakulasuriya produced a valuable report that evaluated the evidence for the implementation of screening for oral cancer in the UK against the National Screening Committee (NSC) criteria [16]. The report suggested that there is still considerable uncertainty around the natural history of the disease and thus, a UK national screening programme cannot be advocated. The review by Warnakulasuriya and Cain [17] also highlighted the need of further research in several specific and key areas to justify the establishment of a nationwide screening programme. The review suggested that more research is required to identify early disease markers to understand the disease progression and to find the best test available for the earlier detection of the disease. The necessity of additional studies in primary care settings to define the values of already existing tests, and the identification of the most sensitive and specific test on offer were also emphasised in the review. Evidence from the recently updated Cochrane review on oral visual examination (OVE) as a part of a population based screening program for oral cancer reported improved survival and a significant stage shift to diagnosis of early stage disease across the population as a whole, and a 24% reduction in mortality in high-risk groups (males who used tobacco and/or alcohol) [18]. However, the findings of the review were based on one randomised trial conducted in a high prevalence population in Kerala, India, so its generalisability to a Western population is uncertain. In the UK, General Dental Practitioners (GDPs) currently hold the main responsibility for the early detection of oral cancer [19]. It appears likely that GDPs should detect more cases of oral cancer opportunistically than General Medical Practitioners (GPs) because GDPs’ examine the oral cavity regularly. However, it has been reported that where patients do present with symptoms, only 40% of such presentations are to the GDPs [20]. In a widespread GP Patient Survey conducted between July to September 2013 in the UK, 1.3 million adults were asked about access to NHS dentistry. A total of 450,000 adults replied, of whom only 57% visited for dental check-ups in the previous two years [21]. As high-risk individuals (those who smoke tobacco, regularly drink alcohol and are over 45 years old) comprise the least likely cohort to be regular attendees for dental check-ups [22,23], opportunistic screening for oral cancer, if focused only on the dental examination, may miss a large proportion of this high-risk population [24]. As these high-risk individuals are more likely to visit general medical physicians than dentists, primary care may provide the opportunity for detection of potential cases of oral cancer. Evidence to date also concurs that the most cost-effective method of screening would be opportunistic programmes targeting high-risk individuals attending primary care [3]. For any screening programme to be established, it is essential that the programme should be acceptable to the patient and the benefits of the screening programme must outweigh the physical and psychological harm to the patient such that the patient is willing to engage with the programme. There has been a plethora of research on patient delay on oral cancer [7,25] and cost effectiveness of a UK wide oral cancer screening programme [3]. However, there is a paucity of studies looking at patients’ preferences, satisfaction and willingness to undergo oral cancer screening, especially in non-dental care settings. Patient’s preferences and perspectives are important in successful tailoring of screening services. This systematic review aims to determine the acceptability of screening for oral cancer outside of dental care settings. We believe that the synthesis will contribute to the evidence in determining the feasibility of an opportunistic screening programme in the UK.
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Materials and methods Eligibility criteria Studies were eligible if they (i) reported acceptability of oral cancer screening to undiagnosed individuals (ii) included primary data; (iii) were published in English. Studies were excluded if they only focused on healthcare professionals’ attitudes towards screening of oral cancer, referred to malignancies outside the oral cavity and screening for cancer in general, focused mainly on patients’ acceptability of diagnosis of oral cancer as opposed to detection, and/or compliance with specialist care, and those that were carried out in dental settings. Information sources and search We searched EMBASE, MEDLINE, Cochrane Database of Systematic Reviews, CINAHAL, psycINFO, CANCERLIT and BNI to identify relevant articles published between 1975 and Dec 2013. References in each of the identified articles were further screened for relevant references. Three comprehensive search themes were used while conducting the search in the electronic databases: (ii) identification of the relevant disease of interest, i.e. oral cancer, and (ii) identification of the relevant terms for screening and (iii) identifying the relevant terms related to acceptability and satisfaction. We then combined the results of the searches using the Boolean operator AND (Fig. 1). Study selection and data extraction Two reviewers (PP and FF) independently carried out the search, screened the titles of the articles and removed any irrelevant and duplicate articles. Abstracts of the remaining articles were assessed applying the inclusion criteria. Any disagreements in selections were discussed and resolved during consensus meetings involving a third investigator (CL). Relevant studies are presented in Fig. 2. We extracted the relevant information from the selected studies: study ID, study aim, sample characteristics, study design and number of participants, data collection method and period and key factors indicating screening acceptability to patients. The results are summarised in Table 1. Results A total of 2935 references were initially identified from the computerised search but 2217 were excluded after screening the titles. From the abstracts of the remaining 178 articles, 47 full text articles were retrieved for further scrutiny, and 12 studies were found to be eligible for inclusion. The study design varied across the studies; five were cross sectional [26–30], three were randomised controlled trials (RCTs) [31–33], three were focus group and/or interviews [34–36], and one pre-post design [37]. The majority of the studies (n = 7) were conducted in the UK [28,30–34,36], two in the USA [35,37], one in Canada [29] and two in India [26,27]. The details of the included studies are provided in Table 1. Factors associated with the acceptability of oral cancer screening Preference for care provision Three studies evaluated patients’ preferences for care provision for oral cancer screening [34–36]. In all three studies, participants stated their preference for having primary care physicians perform the oral cancer examination. General practice was seen as an appropriate setting for screening due to its local nature, ease of
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Fig. 1. Terms used to search the electronic databases.
access, familiarity and relevance for a health-related intervention [34,36]. Participants stated their preference for receiving information about oral cancer through personal interaction with their primary care practitioners [34]. Lack of trust towards dentists was stated as a barrier in one study where participants perceived a dentist as a ‘tooth specialist’, rather than a ‘mouth specialist’, who lacked the power of a doctor to make referrals and write prescriptions [34]. Cost and related factors Financial cost was perceived as an influencing factor for the acceptance of screening. In Dodd et al. [35], willingness to accept a free oral cancer examination was high among males (100%; n = 32) whereas younger females did not uniformly agree with the idea. The females in the study stated that they would decline the opportunity to be screened even if screening was conducted at their worksite and offered free. Participants in another focus group study also perceived that the screening should be cost free and speedy [34]. However, there were stark differences in participants’ characteristics, cultural beliefs regarding oral cancer, and health care provision across these two studies conducted in different countries, which may have affected participants’ opinion about the financial cost related to screening.
Knowledge and awareness of oral cancer It was frequently reported that patients had inadequate knowledge about signs and symptoms of oral cancer [34–37] and a lack of awareness of the importance of a recommendation for oral cancer screening [34,35]. In one study conducted amongst a high-risk population in Canada, 88% of the participants were unaware of the disease [37]. However, in a study from India, the overall awareness of oral cancer of study participants was over 80% following health education using the Mouth Self Examination (MSE) brochure, leading to 95% of participants correctly identifying the different risk factors [26]. The need for more public information about oral cancer was also reported in some studies [35,36]. Interventions such as written information materials provided to patients in primary care were reported to have the potential to boost immediate knowledge levels of oral cancer, thus resulting in increased intentions towards oral cancer screening [32,33]. Anxiety related to symptom and screening procedure Patients perceived that knowing more about oral cancer may make them more anxious should they notice any disease symptom [36]. However, studies aimed at increasing knowledge and awareness of oral cancer reported that access to information does not increase pre-procedural fear and anxiety of participants [31–33].
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Databases searched
2935 studies identified
Screening of titles and abstracts for relevant studies
47 relevant studies identified
Studies read in full and application of inclusion criteria
12 studies selected for inclusion for review.
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Impact of intervention on compliance of screening In one study conducted among a high-risk population in India [26], compliance with instructions to perform MSE following access to an information leaflet was high, with 87% of the participants practising MSE and 95% believing that early detection could improve the chances of cure. Whilst the sensitivity of MSE was very low at 18%, the specificity was high at 99.9% (PPV = 72%, NPV = 99%). In another study, participants underwent an oral examination by their dentist and then performed MSE after reading an instructive leaflet [28]. The study found that half of the participants (51%) correctly diagnosed the symptoms and the majority (74%) of participants found MSE easy to perform. However, the sensitivity and specificity of MSE was 33% (95% CI 11–65%) and 17% (95% CI, 6–40%) respectively. Perceived benefits of and barriers to oral cancer exam Patients perceived that screening would be helpful to detect disease early, and would lead to longer life, peace of mind, prevention and awareness [35,36]. Lack of awareness of oral cancer, the belief that oral cancer is rare, uncertainty of the exam process, fear of pain, and costs related to oral cancer exam were cited as the major barriers to the oral cancer exam in a focus group study conducted by Dodd et al. [35]. Individuals in this study suggested that there is a need for convenient locations, extended hours in health clinics, mobile clinics, Saturday hours and also a desire for low to no-cost dental examinations. Lack of confidence in performing MSE was stated as another barrier [28].
Fig. 2. Article selection process.
One study reported that information leaflets did not change concerns regarding MSE, although one-to-one interaction sessions were helpful in reducing MSE related anxiety [31]. Similar results were reported in other studies where anxiety associated with the screening was not influenced by leaflet access [33], or were reduced [32]. One study reported pre-procedural anxiety in one third of participants (31%), however, on completion of the screening, there was almost unanimous agreement that the procedure was painless [30].
Socio-demographic characteristics Across the studies, there were no clear relationships between socio-demographic factors and acceptance of screening. The studies were extremely varied culturally and ethnically.
Impact of written information on intention to accept oral cancer screening Two RCTs assessed the influence of Patient Information Leaflets (PIL) on intentions to accept screening (32, 33). Both studies found a positive influence of information leaflets; those receiving a leaflet were more likely to accept an oral cancer screen if offered. The leaflet group also had stronger beliefs that health personnel and family would expect them to accept screening and perceived that screening would be less of a waste of time and not painful [33]. The third RCT assessed the impact of a leaflet and a one-to-one interaction on earlier presentation of oral cancer, including MSE [31]. The study reported that the interventions resulted in an increased knowledge of oral cancer, increased perceived confidence to seek help and perform MSE, and reduced anticipated delay in seeking help for potentially malignant oral symptoms. Rwamugira and Maree [37] found that the quality of the written material affected the individuals’ decision to uptake screening; individuals who found the information easy to understand were more likely to be motivated to take up screening.
Patient experiences and acceptance of specific screening activities The acceptance of oral visual examinations (OVE) conducted in community screening programmes varied across studies. In a study conducted among tobacco users in India, overall acceptance and satisfaction levels of OVE in a mobile setting were encouraging, with 98% of the participants feeling comfortable with oral screening tests [27]. Similarly another study in Canada also reported high acceptance of OVE (98%) among high-risk individuals (based on risk factors, lack of access to care, and the high frequency of oral mucosal anomalies), but, acceptance of biopsy for abnormal findings and follow-up was low with only 12 out of 31 (39%) patients with clinical leukoplakia accepting the biopsy [29]. In contrast, a study from South Africa, reported poor acceptance of OVE conducted in mobile clinics with only 4.9% (out of the 1320 eligible adults in the community) accepting a screen during the 6-week period [34]. Of those who accepted the examination, only 12% were high-risk participants (specified as men older than 40 years of age). Feaver et al. [30] found that the use of Orascreen (a screen using toluidine blue dye) in aiding the screening for oral cancer was highly acceptable to patients; 100% individuals accepted the screening, 83% described screening as ‘a comfortable experience’ and 95% of the respondents expressed a willingness take part in future oral health screening. Discussion This systematic review has considered the available evidence relating to patients’ acceptability of oral cancer screening in nondental settings. Although some attempts have been made to explore patients’ attitudes and responses towards oral cancer screening processes, the acceptability of screening for oral cancer to patients does not appear to have been the specific focal point of any published studies. The overarching theme from the reviewed studies appears to be that, while the potential barriers to screening and diagnosis are diverse, the majority of methods of screening for oral cancer are entirely acceptable to patients per se. Lack of acceptability of screening from the patients’ viewpoint
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Table 1 Details of the studies included in the review in chronological order. Study
Sample characteristics
Study design (No of participants)
Key factors indicating screening acceptability to patients
Zohoori et al. [34]
Male smokers and/or drinkers, irregular dental attenders aged 40–61 years living in economically deprived area of Teesside, UK
Focus group (N = 18)
Scott et al. [31]
Smokers aged between 45 and 65 years recruited from three GP practices in South East London, UK
RCT; patients randomised to three groups, leaflets or one to one instruction or control group. Selfreporting questionnaire at 1 month post intervention (N = 112)
Kumar et al. [27]
Female smokers aged between 30 and 65, India
Interview administered questionnaire after being screened (N = 59)
Elango et al. [26]
Individual aged between 10 and 99 from two adjacent coastal villages in Kerala, India
Interview administered questionnaire at 4 weeks after patients read brochure regarding MSE (N = 34,766)
Scott et al. [36]
Smokers and/or drinkers aged between 45 and 65 years recruited from a GP practices in South East London, UK
Study 1: Semi-structured interviews N = 25 Study 2: Use of ‘think-aloud protocol’; participants read the leaflets and at the same time verbalise their thought and feelings (N = 14)
Rwamugira and Maree [37] Scott et al. [28]
Individual aged 18 and over registered as a client of a Nursing community of practice, USA
Structured interview pre- and post-2 months after nursing intervention (N = 65)
Lack of knowledge and awareness of oral cancer and its signs and symptoms. Preference to be screened by GP and family physicians during routine health checks, and preference for the use of a ‘‘health’’ setting as opposed to a ‘‘dental’’ setting for screening Brief interventions seem to be effective tool to encourage early detection of oral cancer. The intervention groups felt significantly more confident and more likely to perform MSE than the control group High level of acceptance and satisfaction with OVE mobile screening clinic; 98.31% were satisfied with the test procedure and examination room, 100% were satisfied with the privacy level MSE shown to be highly acceptable screening tool but effectiveness questionable; MSE identifies high-risk lesions well (detection of red patches 66.7% but 87% not detected case were of white patches Lack of knowledge; concern about wasting PCP’s time with minor symptoms, lack of confidence in performing MSE although participants found MSE straightforward and easy to follow. GP practice was seen as an appropriate setting for screening Screening uptake was poor (4.9%). The strategy used to improve knowledge and awareness was successful
Smokers aged over 45 recruited from GP’s list in South East London, UK
Self-report questionnaire after performing MSE (participants read information leaflet prior to MSE). Proforma (dentist) (N = 54) Focus group (N = 56)
Dodd et al. [35] Poh et al. [29]
Humphris et al. [32] Humphris and Field [33] Feaver et al. [30]
African Americans aged between 35 and 75 recruited at a private research firm, USA Individuals (mean age 47 years) attending community outreach dental clinic, Vancouver, Canada Participants (mean age 44 years) were recruited from 14 general practices in the north west of England, UK Individuals (mean age 43 years, SD 15 years) were recruited from dental and medical waiting rooms in the North West of England, UK Employees aged between 40 and 59 years in a large retail chain in the UK
Structured individual interviews prior to OVE (N = 204)
RCT; patients randomised either to leaflet or nonleaflet group, a questionnaire completed immediately post intervention (N = 800) RCT; patients randomised either to leaflet or nonleaflet group, a questionnaire completed immediately post intervention (N = 769) Self-reported questionnaire Survey (N = 140)
does not appear to be a significant barrier to carrying out opportunistic screening of high risk populations. Inadequate knowledge about oral cancer and screening processes was common and acted as an obstacle to the uptake of screening. Other barriers included financial and logistical barriers such as cost related to the screening process and transportation. Provision of information about the disease seems to improve knowledge and awareness of symptoms, and have a positive impact on likely acceptance of oral cancer screening [32,33]. Where individuals expressed some fear and anxiety with regard to screening, it was demonstrably lessened by education about the benefits of being screened for the disease. However, it is still unclear whether the effects of these brief interventions translate into significant clinical differences such as earlier diagnosis, treatment and therefore a reduction in morbidity and mortality [31]. Preference for seeking help from GPs rather than from dentists, and preference towards a general practice setting as opposed to dental clinics was stated in many studies, although this bias may reflect the exclusion criteria for the review. Previous studies have indicated that the majority of patients (over 70%) are more likely
The risk groups were poor at correctly identifying the presence or absence of potentially malignant oral lesions. The majority (74%) found MSE to be very easy or easy Lack of knowledge of risk factors and severity of late diagnosis, preference for having primary care physicians perform the oral cancer exam Acceptance of screening was high (98%); however, acceptance of biopsy for abnormal findings and follow-up was low (only 12 out of 31 patients with clinical leukoplakia were biopsied) PIL demonstrated an increase in intention to have an oral cancer screen and reduced anxiety PIL shown to be useful in improving patients’ knowledge of oral cancer and intention to accept an oral cancer screen Anxiety about oral health screen not raised by leaflet exposure Toluidine blue shown to be highly acceptable screening tool
to consult a GP should symptoms arise, and fewer than half to a dentist [38]. In addition, studies conducted in dental settings have reported low uptake (24%) of free mouth checks [39]. This suggests that oral cancer screening in a general practice settings may be more efficient and acceptable to participants. However, to prevent patients and the GP practice being overwhelmed by various interventions for each cancer type, the screening of oral cancer could feasibly be incorporated into a wider early cancer detection programme [31]. Our intention was to review the acceptability of oral cancer screening as a whole rather than specific screening methods. It appears likely that MSE would have high levels of acceptability to patients, as it is free and unlikely to induce the same anxiety as a visit to the dentist. However, MSE is subject to the same hindrances as other screening methods, namely low levels of patient awareness and questionable reliability of results. Any new screening technique or adjunct devices for use in the UK are required to conform to the National Screening Committee (NSC) criteria before being recommended for implementation. These criteria are robust and request evidence for a simple, safe, precise and validated
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screening test that is likely to be acceptable to the population [40]. Individuals were considerably more likely to conduct MSE after education about oral cancer but sensitivity and specificity of the examination were highly variable between studies [26,28]. Nevertheless, the encouragement of MSE is not without its benefits because it is likely to increase overall understanding of oral cancer and bring about earlier presentations as a result. The studies concerning a specific screening method such as Orascreen were highly acceptable to patients but provided no evidence relating to sensitivity or specificity of results [30]. Although we did not specifically look at the diagnostic accuracy of the screening methods, the sensitivity and specificity of the screening methods varied across the studies. In a recent Cochrane review on diagnostic test accuracy of conventional oral examination as a screening test in primary settings, sensitivity estimates ranged from 0.50 (95% CI 0.07–0.93) to 0.99 (95% CI 0.97–1.00) and specificity ranged between 0.98 (95%CI 0.92–1.00) and 0.99 (95% CI 0.99–0.99) [41]. Not much is known about the relationship between test performance and patient acceptability of oral cancer screening, however, high levels of sensitivity and specificity are important as there is a risk of false reassurance for those with false negative results and unnecessary anxiety for those with false-positive results [28]. The overall acceptance and satisfaction with OVE conducted in mobile settings was encouraging in a study conducted in India suggesting that similar screening programmes may be a feasible option in a resource poor setting. However, the screening uptake with OVE mobile clinics was disappointing in another study conducted in Africa indicating that barriers to screening uptake should be explored further and adapted according to the local setting. It is not known how these findings would relate to similar ethnic groups at high risk in the UK. Some variations regarding acceptance and experiences of oral cancer screening were observed according to socio-demographic profile of the participants. This highlights that interventions and strategies should be targeted closely to specific at risk groups. This systematic review is subject to a number of limitations. As there was wide variation in the design of the studies included in the review, we did not assess the quality of the individual study. In addition, studies that were not written in English were excluded. Due to the high incidence of oral cancer in the Indian Subcontinent, it may have been useful to include more literature from this region, potentially in local languages. Nevertheless, this review did include papers from the UK, the USA, South Africa and India. Cultural differences between these countries are likely to have a major effect on both incidence rates and patient attitudes but it has not been possible to explore these differences in detail. In addition, studies that did not focus on oral cancer (as opposed to other cancers) were excluded. Relevant information from studies examining cancer screening in general may therefore have been overlooked. The small sample sizes used in some studies make it difficult to reliably apply the findings to the general population. However, each study acknowledged this limitation. Due to the relatively low incidence of oral cancer in the UK, this limitation appears somewhat unavoidable, particularly in studies where the selection criteria include younger patients. In addition, this review only explored the views of patients who accepted screening. Future studies need to explore reasons for non-uptake of screening which may be helpful to inform interventions to address potential barriers for screening and formulate strategies to facilitate earlier diagnosis of oral cancer, which are acceptable to patients. In summary, the available evidence suggests that acceptance of, and satisfaction with oral cancer screening is high, particularly where patients have previously been educated about oral cancer. This indicates that existing screening methods are generally acceptable, and where they at first appear not to be, the explanation may be a lack of understanding of the screening process rather
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