Abstract
Abstract
Background: Microbial oral biofilms are ecologically diverse, complex, dynamic, and little understood. In health, biofilms comprise balanced microbial communities in symbiosis with their human host. However, environment- and lifestyle-associated ecosystem changes can perturb that balance, resulting in dysbiotic host-biofilm relationships, which support the development of caries and periodontitis. To date, microbial findings on distinct oral biofilms and the relative abundance of key oral bacteria in a prospective birth cohort have not yet been reported. Aims: This study aimed to: (1) identify and enumerate 30 ecologically- and clinically-important oral bacterial species in four distinct oral biofilms; (2) investigate associations between key oral species and caries and periodontitis; and (3) evaluate the importance (and possible influence) of putative host-modifying risk factors (such as long-term exposure to oral biofilms and smoking) on biofilm microbial composition. Methods: Oral biofilm samples were collected from four habitats from 841 Dunedin Multidisciplinary Health and Development Study members at age 32. The resultant 4500 samples were analysed using checkerboard DNA-DNA hybridisation (CKB), focusing on 30 key oral bacterial species. The CKB data were used to describe habitat-specific biofilm species profiles and evaluate the importance of sex, smoking and oral hygiene. Associations of CKB data with caries at age 32 and caries increment between age 32 and age 45, were assessed using regression modelling. Longitudinal periodontitis extent data were used in the group-based trajectory modelling. This modelling assigned participants to periodontitis trajectory groups. Associations of CKB data with periodontitis trajectories were assessed using multinomial logit function. Results: Habitat-specific biofilms, shaped by discrete microenvironments, varied widely among individuals. Each habitat biofilm had a distinct microbial profile which differed by sex, smoking status and oral hygiene, and with differing experience of caries and periodontitis. Higher averaged proportions of supragingival biofilm species—such as Tannerella forsythia and Micromonas micros, caries pathobionts and commensals—were associated with untreated caries at age 32 and with caries increment from age 32 to 45. Higher proportions of Leptotrichia buccalis in all the biofilms—and of health-associated species, periodontal and caries pathobionts in the posterior supragingival biofilm—were associated with periodontitis. Sustained poor oral hygiene through to age 32 was associated with greater caries experience by age 32 and with greater incidence of new caries from age 32 to 45 years. Environmental and lifestyle risk factors such as poor oral hygiene, smoking rate and duration, and low socio-economic status were associated with a higher likelihood of having periodontitis. Conclusions: The shift from homeostasis to dysbiosis in cariogenic and periopathogenic biofilms is dynamic and variable, highlighting that they are more than the sum of their constituents. The study findings support the usefulness of contemporary CKB analysis data for characterising oral microbiota biofilms in a large-scale epidemiologic study. They also support the polymicrobial aetiology of caries, the polymicrobial synergy and dysbiosis periodontitis aetiological model, and the integrated hypothesis of caries and periodontitis. They reinforce the substantial effects that sustained poor oral hygiene, xerostomia, low socio-economic status and smoking exposure have on oral health and add to the understanding the natural history of caries and periodontitis.