Exploring the relationships between periodontitis, high-risk oral human papillomavirus and social factors and their impact on oral health status in Indigenous South Australians

Abstract

Aboriginal and Torres Strait Islander people (hereafter referred to as Indigenous people) have been living and practicing diverse cultures on the continent of Australia for more than 60,000 years. Yet following colonisation in the 1700s, Indigenous people have experienced continued oppression, marginalisation, and dispossession from land and culture, that manifests in unacceptably adverse health and wellbeing outcomes. This includes experiences of poor oral health, with high rates of dental caries, periodontitis, oral cancer and human papillomavirus (HPV)-positive oropharyngeal squamous cell carcinoma (OPSCC) in Indigenous Australians when compared with non-Indigenous Australians. Indigenous people also access oral healthcare differently. They are less likely to visit a dentist for a routine dental check-ups and therefore less likely to receive preventive dental care, instead presenting more often with a dental health problem or established oral disease. Given the high burden of oral health conditions there is a strong need for strengthened efforts to promote preventive approaches related to oral health among Indigenous Australians. This includes a greater understanding of the etiological factors of emerging oral conditions such as HPV-positive OPSCC, which has high mortality rates because it is commonly discovered at a late stage. HPV vaccination programs remain an important OPSCC control strategy, however HPV vaccines provide little protection to individuals already exposed to HPV infection. This is why new approaches to screening are required to permit early detection, and management of OPSCC, particularly in high-risk populations. One of the most consequential oral diseases for health and quality of life is periodontitis, which results in multiple tooth loss, edentulism and masticatory dysfunction, and disproportionately affects Indigenous people. Emerging data suggests a possible role for periodontitis as reservoir for latent oral HPV infection. Detection of periodontitis may thus identify individuals at increased risk of persistent infection and OPSCC, who may benefit from increased surveillance. The high burden of both periodontitis and HPV-positive OPSCC in Indigenous people indicates that Indigenous people may have great potential to benefit from improved screening for periodontitis and OPSCC; however, research is needed to confirm or refute a link between these conditions. Given the high burden of oral disease, it is also important to understand the broader proximal and distal factors affecting oral disease and oral health related quality of life (OHRQoL). Racism is known to negatively impact on the general health of an individual and there is emerging evidence that racism has adverse effects on oral health and OHRQoL. However, to date, the impact of racism on OHRQoL among Australian Indigenous people has not been studied systematically. It is important to understand this link further to determine the need to address racism in broader oral health promotion strategies. Lastly, the inequities in oral health outcomes experienced by Indigenous people in Australia are thought to be underpinned by a complex interplay of social factors that reflect social disadvantage, poorer health literacy, a lack of awareness regarding oral health preventive programs, experiences of racism and limited availability of oral healthcare that is culturally relevant. To date, there has been limited in-depth investigation of barriers faced by Indigenous people with regard to seeking oral healthcare services, particularly preventive services. This area needs further exploration to understand experiences of oral healthcare and therefore opportunities to improve engagement with care and to reduce oral health inequities. This thesis focuses on several key oral health areas that disproportionately affect Indigenous people and are understudied in this population. The thesis addresses key gaps in understanding about 1) the relationships between periodontitis, oral HPV and HPV-positive OPSCCs, 2) the relationships between self-reported periodontitis and oral high and low-risk HPV infection specifically among Indigenous people, 3) the influence of self-reported racism on OHRQoL among Indigenous people, and 4) factors that affect Indigeonus people seeking and accessing oral healthcare. The aims of this thesis are to: 1. Examine the strength and quality of the overall evidence concerning the relationships between periodontitis, oral HPV infection and OPSCC; 2. Examine the association between self-reported periodontitis and oral high and low-risk HPV infection specifically among Indigenous South Australian adults; 3. Determine if self-reported racism is a risk factor for poor OHRQoL among Indigenous South Australian adults; and 4. Explore experiences of and the factors that influence Indigenous people’s use of oral healthcare services. Methods: 1. A systematic review and meta-analysis was conducted capturing all published studies up to 12th February 2020 evaluating the association between periodontitis and separately, oral HPV infection and OPSCC. 2. Analysis of baseline and 12 month follow-up data collected as part of a prospective cohort study known as the ‘Human papillomavirus and oropharyngeal cancer among Indigenous Australians’ study, involving 1011 (at baseline) Indigenous South Australians (SA) aged 18+ years recruited between February 2018 and 2020. Detailed information on sociodemographic characteristics, health-related behaviours, and sexual history were collected at enrolment. Saliva samples were collected and tested for the presence of oral HPV DNA using the optimized general primer (GP) + PCR system. The primary outcomes were the prevalence of any high-risk oral HPV DNA and the prevalence of HPV 16 and/or 18, separately. Periodontitis was assessed using validated, self-reported periodontitis screening questions. 3. Analysis of data collected in the ‘Human papillomavirus and oropharyngeal cancer among Indigenous Australians’ study at enrolment that included social background, connection to culture and cultural values, utilization of dental services, and OHRQoL; the latter was captured using the Oral Health Impact Profile (OHIP-14). We defined the dependent variable ’poor OHRQoL’ as the presence of one or more OHIP-14 items rated as ‘very often’ or ‘fairly often’. Experiences of racism were also evaluated using the Measure of Indigenous Racism Experiences instrument. Interpersonal racism was classified into two categories (‘no racism’ vs. ‘any racism in ≥ 1 setting’) and three categories (‘no racism’, ‘low racism’, and ‘high racism’). 4. A qualitative study was undertaken with 19 Indigenous people living in different regions of South Australia including Adelaide, Port Augusta, Mount Gambier, Whyalla, Port Lincoln, and Port Pirie. Participants were identified through existing participation in the ‘Human papillomavirus and oropharyngeal cancer among Indigenous Australians’ study. Purposive sampling was undertaken to ensure variation in sample with respect to geographic location, gender and age group. The interviews were undertaken by an experienced Indigenous researcher, who was present in person with the participant, and a non-Indigenous researcher (Ph.D. candidate) who joined the interview remotely via video conferencing services. Interviews were transcribed, coded line-by-line and analysed using an inductive thematic approach to generate key themes, which were then checked and refined with the Indigenous researcher and the supervisory team. Theme development was informed by existing frameworks concerning social and cultural determinants of oral health, including the framework by Patrick and colleagues (2006). Results 1. The systematic review identified 13 studies; four case-control and nine cross-sectional. Of these, five studies could be included in the meta-analyses. There was no significant increase in the odds of high-risk oral HPV infection among individuals with confirmed periodontitis (odds ratio (OR): 4.71; 95% confidence interval (CI): 0.57–38.97). Individuals with periodontitis had a 3.65 (95% CI: 1.67–8.01) times higher odds of having any type of oral HPV infection compared with those without periodontitis. The overall body of evidence was rated as low to very low certainty. There were insufficient studies to robustly evaluate the relationship between periodontitis and HPV-positive OPSCC. 2. Among the 673 participants with sufficient data for analysis, 17.1% had self-reported periodontitis, 5.9% had any high-risk oral HPV and 2.1% had oral HPV 16 and/or 18. Among those who self-reported periodontitis, any high-risk oral HPV was detected among 17.5% participants and oral HPV 16 and/or 18 was detected in 21.4%. Logistic regression analyses revealed no significant association between self-reported periodontitis and either any high-risk oral HPV (adjusted OR: 1.10; 95% CI: 0.45–2.70) or oral HPV 16 and/or 18 (adjusted OR: 1.27; 95% CI: 0.32–5.03). 3. Among the 885 participants with sufficient data available for analysis, 50.2% reported poor OHRQoL and 52.1% reported experiencing any interpersonal racism in the previous 12 months. Relative to having no experiences of racism in the previous 12 months, those who experienced any racism (≥ 1 setting) were significantly more likely to report poor OHRQoL (adjusted OR: 1.43; CI:1.08–1.92). The odds of having poor OHRQoL among females experiencing racism were 1.74 times higher (95% CI: 1.07–2.81) than among males. 4. Thematic analyses identified individual, interpersonal, community and macro-level factors that influence Indigenous people to seek and access oral healthcare overall and preventive care specifically. Key obstacles to seeking care identified by participants included fear and shame, negative past experiences and oral health misconceptions at the individual level and personal stressors and racial discrimination at the interpersonal level. Accessibility of services and the degree of community-based services and support from community members were identified as important factors at the community level. At the macro level, complex processes relating to financing and reimbursement for oral healthcare as well as workforce shortages were important impediments to use of oral healthcare services. Conclusion Findings of this thesis have demonstrated that there is an association between periodontitis and any HPV infection overall. However, the relationship with high-risk HPV is less clear, in part reflecting low certainty evidence. When studied specifically among Indigenous South Australians, the association between periodontitis and any or high-risk HPV could not be confirmed. This suggests that periodontitis may not be a useful marker to identify those at high-risk of OPSCC. Further research that includes a clinical diagnosis of periodontitis could help in clarifying the role of periodontitis in the acquisition and persistence of high-risk oral in communities with high disease prevalence. This thesis has also demonstrated an association between racism and poor OHRQoL, suggesting the need for culturally sensitive strategies to overcome the experiences of racism among Indigenous Australians while seeking oral healthcare. In-depth analyses identified various individual, interpersonal, community and macro-level factors that affect oral healthcare seeking behaviour in this population. Collectively this indicates that strengthening preventive approaches to oral health for Indigenous people requires dedicated strategies to make oral healthcare more accessible and culturally sensitive. Sustained funding for oral healthcare and oral health literacy initiatives, co-design of services with Indigenous people and increasing the number of Indigenous people in the oral healthcare workforce are critical steps forward in this regard.