The One Health Approach to Q Fever Prevention and Control in South Australia

Abstract

Background Q fever is a zoonotic disease, transmissible from animals to humans, and has potential for community outbreaks. Despite the availability of a human vaccine, Australia continues to bear a substantial burden of Q fever among at-risk populations such as abattoir workers, livestock farmers, and wildlife workers. A One Health approach, which engages crosssectoral collaboration among human, animal and environmental health sectors and creates mutually benefiting outputs for all, is an appropriate framework to consider for Q fever prevention and control. Q fever epidemiology is complex because of the involvement of multiple species in disease transmission, presence of ticks in the environment that constantly serve as a vector transmitting Coxiella burnetii between wildlife and livestock, and the proximity and interactions of humans to animals through an array of practices including farming, meat processing or even shooting. Given the extent of agricultural practices humans are involved with, there may be associations between livestock densities and spatial clustering of human cases. However, evidence concerning the spatial relationship between cattle, sheep and goat populations and human Q fever cases is still relatively scarce. Given the inherent occupational risks of Q fever for unvaccinated animal and veterinary science students and livestock farmers, assessment of their perspectives on Q fever prevention using a One Health framework is important because evidence suggests that they are at risk, however, little is known about the extent of that risk. Finally, exploring Australian general practitioners’ (GPs’) and broader health systems’ preparedness for Q fever prevention through the analysis of multi-stakeholders’ perspectives on the constituents of an effective systemic approach to disease prevention and the potential affordances of a One Health framework may attract considerable interest for guidelines and recommendations for policy. Aims The thesis is divided into six studies each with specific aims. Study 1, a literature review, aimed to assess whether components of One Health have been utilized for Q fever prevention and control in Australia and internationally. Study 2 aimed to analyze Q fever notification data in order to define at risk groups based on occupation and possible exposure in South Australia (SA). In this study, the association between notified Q fever cases and the spatial and temporal distribution of cattle, sheep and goats in SA was examined. Studies 3 and 4 aimed to assess the knowledge, attitudes and practices about Q fever and its prevention among university animal and veterinary science students, and livestock farmers in SA, while study 5 compared and contrasted the varying perceptions of Q fever and its prevention between students and farmers. Finally, study 6 aimed to explore multi-stakeholders’ perspectives for identifying barriers and enablers of a One Health approach to Q fever prevention and control. An overall aim was to examine Q fever control and prevention approaches in SA, and to explore the enablers and barriers of adopting a One Health approach in order to provide policy recommendations and guidelines. Methods Study 1 involved a literature review of published studies on Q fever that utilized one or more components of a One Health approach. Study 2 was an epidemiological review of Q fever notifications between January 2007 and December 2017 obtained from the Communicable Disease Control Branch, SA Department for Health and Wellbeing (CDCB, SA Health). Notification rates and incidence rate ratios were calculated. Additionally, spatial mapping of Q fever notifications was undertaken using livestock density data and the locations of abattoirs and saleyards in SA. Studies 3 and 4 were an online survey of animal and veterinary science students enrolled at the University of Adelaide (UoA), and members of Livestock SA representing cattle, sheep and goat farmers in SA to gauge their perceptions about Q fever and its prevention. Descriptive analysis and logistic regression were used in studies 3 and 4. Study 5 collated the open responses from studies 3 and 4 concerning suggested strategies for Q fever prevention. Thematic analysis was performed to identify emerging themes. Study 6 included semi-structured interviews among participants drawn from four stakeholder groups including GPs and veterinarians who play a key role in Q fever surveillance; SA Health and SafeWork SA representatives who have roles and responsibilities concerning Q fever policy and guidelines; researchers from UoA and the University of Queensland concerning evidence and current preventative practice; and representatives from Livestock SA and NSW farmers whose suggestions are instrumental for industry specific tailored recommendations. A qualitative approach was undertaken to analyze emerging themes concerning Q fever diagnosis, notification, and control and prevention including vaccination. Results In study 1, seven major themes were elicited from the literature review including human risk assessment, human and animal serology, integrated human-animal surveillance, vaccination for at-risk groups, environmental management, multi-sectoral collaboration, and education and training as important components of a One Health approach. In study 2, 167 Q fever cases were reported in SA during 2007–2017, and rates (1.52/100,000) were higher among males (72%) aged 21–40 years, with 22% of notifications recorded in a suburb containing an abattoir. Commonly reported occupations were livestock farmers (35%), abattoir workers (20%) and individuals with no known occupational risks (15%). Eight cases (5%) reported prior vaccination for Q fever. Annual goat, cattle and sheep counts were highly correlated with each other (P < 0.001), but none of them, or the total number of livestock were associated with Q fever notifications (P ≥ 0.370). In study 3, 46% of animal and veterinary science students reported limited knowledge of Q fever. Most respondents (96%) reported moderate-high level exposure to high-risk animals. Among animal science students who reported vaccination status, 61% were not vaccinated for Q fever. Identified barriers to vaccination included cost, time and access to healthcare with strategies aimed at promoting awareness, improving healthcare access and subsidized and mass vaccination. In study 4, 80% of livestock farmers who completed the survey had been farming for ≥ 20 years, with sheep and beef cattle their primary stock. The majority of farmers (71%) had good knowledge of Q fever, and 97% were aware of availability of a human vaccine. Despite 95% of farmers acknowledging that the vaccine was effective against Q fever, 42% remained unvaccinated. Identified barriers to vaccination included poor access to a trained doctor and time and cost related to vaccination. Subsidized vaccination and improved awareness were considered to be important strategies for promoting vaccine uptake. In study 5, similar barriers and strategies were highlighted although the main themes identified differed between students and farmers. While students were more focused on the issues around cost, farmers emphasized the importance of the vaccination and were concerned about having access to an accredited GP and GPs’ knowledge about Q fever. In study 6, six major themes emerged including understanding Q fever burden, effective surveillance, the role of general practitioners and other stakeholders, barriers and enablers of vaccination, an integrated approach, and increased Q fever awareness. Participants highlighted that the role of GPs is instrumental in diagnosing Q fever, reporting of Q fever cases to CDCB, and treatment and prevention through health promotion and vaccination. However, the stakeholders also reported that GPs possessed limited knowledge and awareness of Q fever, and believed that leadership was required from SA Health to foster communication, collaboration, and the inclusion of GP networks within an inter-sectoral approach. Conclusions and recommendations While reviewing the literature, significant variation was noted in the practices of a One Health approach to Q fever prevention. Nevertheless, most studies highlighted multi-sectoral collaboration as the key to successful Q fever prevention programs. Higher Q fever rates among young males highlighted a workforce with a high turnover of staff, a transient workforce and possibly under vaccinated, which was consistent with abattoir workers’ profiles, suggesting value of vaccinating this group. Individuals who developed Q fever after vaccination raised concerns about waning immunity or vaccine efficacy, requiring longitudinal studies to assess the degree of immunity conferred by the vaccine. Animal and veterinary science students possessed limited knowledge about Q fever transmission. Their adherence to biosecurity guidelines, a One Health principle, could potentially reduce zoonosis including Q fever transmission. Universities should promote Q fever vaccination among both animal and veterinary science students with possible subsidies. Despite livestock farmers possessing good knowledge about Q fever, biosecurity measures were poorly practiced, and hence adherence to these practices may reduce their chance of contracting the disease. Government and industry partnerships are recommended to promote Q fever awareness, train GPs, subsidize vaccination, and increase its uptake among livestock farmers. Updating medical curricula could potentially enhance clinical understanding for health practitioners. It is prudent to suggest that SA Health should lead the existing zoonosis working group while encouraging active participation from all relevant stakeholders fostering inclusiveness and less power disparity. Further research is required to identify potential options around funding and data sharing between departments for seamless delivery of Q fever prevention services. Although a One Health framework is not devoid of challenges, opportunities for implementation will enhance Q fever prevention programs’ effectiveness.