This study is the first to analyse the prevalence, associated risk factors and geographical distribution of MRS carriage in South East Queensland, Australia. We identified a carriage rate of 8.7% for MRSP and 0% for MRSA in dogs. No MRS was isolated in cats or horses. These findings are in agreement with a recent study in two Sydney veterinary hospitals that isolated MRSP from 8% of veterinary personnel owned dogs and 7% of general canine hospital admissions (32). Other studies in non-clinical Australian settings have yielded much lower MRSP carriage estimates; only one MRSP was isolated from 117 healthy dogs in Victoria (33) and no MRSP on dogs from remote Aboriginal communities in Western Australia and New South Wales (34, 35).While the Victorian and Sydney study did not detect MRSA in cats or dogs, the two studies on dogs from remote Aboriginal communities in Western Australia and New South Wales identified MRSA in 2.6% of the dogs (34, 35). MRSA has been detected in Australian horses (3.7%) (2) so perhaps the lack of MRSA isolation in horses could be explained by the small sample size and single sampling location in this study, indicating the need to enrol more horses from multiple locations in future carriage investigations.
Our results also agree with existing literature from others countries where carriage rates of MRSP in dogs ranged between 3–34% for studies reported from Spain, Finland, Iran and Canada (15, 36–38). MRSP is isolated less often in cats with carriage prevalence between 4–19% as reported in the United States, Brazil and Iran (38, 39, 40). There is currently no MRSP carriage being reported in horses; however, it has been identified from clinical infections (41–43). The low isolation rate of MRSA in dogs and cats was also expected. The reported prevalence of MRSA carriage in dogs ranges between 0.5–9% in Canada, Portugal and the United Kingdom (6, 44–46). A lower prevalence of MRSA ranging between 0–4% has been reported in cats from Brazil, Portugal and the United Kingdom (6, 46, 47). MRSA reported in horses is 2–5% in Canada and the United Kingdom (46, 48).
Our findings suggest that MRSP carriage in dogs is associated with previous history of health-care contact including prior hospitalisation, prior bacterial infection and consultation type. The causal link between MRSP carriage and previous hospitalisation and prior bacterial infection is likely to be confounded by the frequency and length of stay. Indeed, previous studies on risk factors for MRS infections had demonstrated an increased risk linked to more frequent and longer admissions to veterinary clinics (37, 49, 50). This can partly be explained by the increase the likelihood of being exposed and colonised by nosocomial bacteria such as MRS as a function of longer periods spent in healthcare settings or the influence of treatments. Specific consultation types, internal medicine and dermatology, seemed to influence carriage. MRS positive dogs that visited dermatologists had odds twice as high as MRS positive dogs attending internal medicine consultations. Resistant staphylococci are predominately a skin pathogen and are frequently treated by dermatologists (51). Dogs visiting dermatologists are more likely to have a history of persistent MRS infections and increased exposure to antibiotics and corticoids, which could increase the likelihood of MRS isolation from these animals (52). Another point to consider is that higher risks of carriage associated with hospitalisation and dermatology/internal medicine visits do not necessarily mean that transmission is occurring at these locations as dogs visiting these facilities usually experience underlying diseases that expose them to antimicrobials which may facilitate resistance in methicillin susceptible S. pseudintermedius already carried on their skin. This is supported by our finding that dogs with previous bacterial infections had higher odds of carriage. A previous study also indicated that MRSP carriage was higher in dogs that had pyoderma either previously or during sampling (52).
Our analysis is the first to reveal important ecological risk factors associated with MRSP carriage. Precipitation and human population was shown to influence MRSP carriage in dogs suggesting that the environment may play an important role on MRSP in dogs. Our results indicate that increased precipitation is a risk factor for MRSP carriage. Wang, Towers (53) found that average temperature and humidity was significantly associated with S. aureus skin and soft tissue infections in children under 19 years. MRS carriage was significantly associated with temperature and elevation in the univariable analysis (p < 0.20) in our study, but this association was lost after accounting for individual and environmental factors in the final multivariable analysis. The Bayesian analysis, however, revealed that they had a stronger effect on carriage (Supplementary table 2) compared to precipitation and human population. These results indicate a need to investigate further to determine whether temperature and elevation do in fact influence MRSP carriage in dogs. Even though temperature was not significantly associated with MRSP carriage in our dog population, precipitation might serve as a proxy for humidity in this case. Perhaps moisture is influencing the occurrence of bacterial colonisation or infections. In our study, another environmental factor influencing carriage was human population density. High human population could function as a proxy of a higher pet dog population density. Crowds have been known to be at higher risk of bacterial infections, and so the higher density in human and associated dog populations could result in higher skin contact rates between individuals thus facilitating the dissemination of MRSP through the population (54).
Our findings also demonstrate that MRSP is highly clustered in southeast Queensland. After adjusting for individual, clinical and ecological risk factors our results still indicated the presence of residual spatial autocorrelation in MRSP carriage with average cluster sizes of 6 km. The propensity for clustering increased from 47–69% when environmental variables were included in the analysis. This result indicates that MRSP transmission is likely to be spatially structured and could be driven by other environmental or behavioural factors not included in our models. MRSP can be transmitted between and persist in household pets and can survive in the environment for prolonged periods of time (55). These factors could result in transmission in the community outside of the hospital environment such as dog parks or beaches. Indeed, our predictive probability of MRSP carriage map (Fig. 2) indicates that there is higher risk of carriage along the eastern coast of Queensland from the Gold Coast to the Sunshine Coast. Risk also increases north along the coast, which is where average precipitation and temperature are higher too. These high-risk areas included the Brisbane City council, Sunshine Coast council, Noosa Shire, and Gympie regional council. Surveillance strategies associated with MRS in companion animals in South East Queensland should target these areas first. The uncertainty in the spatial prediction (as measured by the standard deviation (SD)) associated with the Brisbane and Sunshine Coast high-risk areas are low (SD: <0.20 to 0.26), which indicates a higher level of certainty associated with these results. The areas with high uncertainty (SD: >034) surrounding the predictions were linked to the northern areas, including Noosa Shire and Gympie, where predicted carriage was between 50 and over 70%. Higher uncertainty (SD: >0.28–0.3) was also associated with the Gold Coast area where there was a high predicted risk of carriage. These areas should be targeted by future sampling studies to fill the gap in knowledge.
The results of our study should be interpreted in light of some limitations. First, there could be bias associated with the clinical sample of individuals we had available for our study. The inclusion of dogs presenting to referral and teaching hospitals might not be entirely representative of a typical dog population. Further, medical records are characterised by incomplete information, which could have contributed to the lack of data for areas found to be associated with high predictive uncertainty for MRSP carriage in South East Queensland such as the Gold Coast and Northern Sunshine Coast. Future studies should aim to investigate MRS carriage in companion animals in this part of Australia. Nevertheless, the findings from this study are useful to uncover the landscape epidemiology of MRS carriage in Australian dogs. Second, the ecological nature of our model could have contributed to a lack of statistical support for the socioeconomic variable which as previously been postulated to be an important factor in antimicrobial resistant bacteria epidemiology, including MRSA (56, 57). While SEIFA scores were significant at the univariable analysis the fact that the SEIFA scores were available at the postcode level could have contribute to the loss of statistical support due to presence of regression dilution bias (58). Further studies should consider obtaining detailed information of owners SES to account for the variation in MRSP risk identified in this study. In addition, our results indicate that our model failed to account for all the residual geographical clustering of MRSP and future studies should consider adjustment for additional finer-scale factors that could influence MRSP carriage status in dogs such as in-house pet contacts, presence of an MRSP infected dog, use of disinfectants at home, as well as human carriage.