Burden and predictors of Staphylococcus aureus and S. pseudintermedius infections among dogs presented at an academic veterinary hospital in South Africa (2007–2012)

Introduction

Staphylococcus bacteria are commensal organisms of mucosal surfaces and skin of both humans and animals but are also associated with a variety of diseases. The organisms can survive for months on environmental surfaces and serve as sources of infection (Neely & Maley, 2000; Coughenour, Stevens & Stetzenbach, 2011). Transmission from dogs to humans occurs following exposure to carrier or infected dogs (Pantosti, 2012; Faires, Tater & Weese, 2009; Frank et al., 2009; Boost, O’Donoghue & Siu, 2007). Due to this risk, some authors have recommended that, where possible, contact between animals and humans should be restricted to mitigate the risk of infection and its associated public health concerns (Faires, Tater & Weese, 2009).

Staphylococcus spp. in dogs have been isolated in several clinical conditions including: pyoderma, otitis, wound infections, sepsis, nasal infections, pneumonia, nephritis, and post-surgical infections (Weese & Van Duijkeren, 2010; Kawakami et al., 2010; Cohn & Middleton, 2010; Ishihara et al., 2010; Kramer, Schwebke & Kampf, 2006; May et al., 2005; Frank et al., 2003). However, the majority of infections have been associated with canine dermatologic conditions.

Due to the high rates of colonization of dogs with Staphylococcus pseudintermedius and Staphylococcus aureus, these species make up the majority of Staphylococcus related infections in dogs. For example, studies conducted in Canada, Hong Kong and Japan have reported the prevalence of S. pseudintermedius in dogs as ranging between 61% and 89.5% (Kawakami et al., 2010; Boost, O’Donoghue & Siu, 2007) whereas the prevalence of S. aureus ranges from 9% to 40% in dogs (Hanselman et al., 2009; Boost, O’Donoghue & Siu, 2007). Dogs also get infected with other species of Staphylococcus such as S. schleiferi, S. epidermidis, S. xylosus and S. felis (Chanchaithong et al., 2014).

There is paucity of information on the epidemiology of staphylococcal infections in dogs in South Africa. Specifically, there is no evidence of studies that have attempted to investigate temporal patterns of infections and the predictors of staphylococcal infections in dogs in South Africa. Furthermore, many of the investigations of predictors of infections described in the literature are based on the analysis of binary outcomes using logistic regression models, and there is no evidence of studies that have tried to ascertain if the predictors of the various Staphylococcus species differ using multinomial models. Therefore, the objective of this study was to investigate the burdens of these infections and use multinomial regression to examine the associations between infection with various Staphylococcus spp., and the demographic and temporal factors among dogs admitted to an academic veterinary hospital in South Africa.

Materials and Methods

Results

Isolated Staphylococcus species

Of the 1,497 samples tested, 26.5% (396/1497) were positive for Staphylococcus spp. From the submitted diagnostic samples, S. pseudintermedius was isolated most often (19.0%, 284/1497), followed by S. aureus (3.8%, 57/1497), unspeciated Staphylococcus (2.9%, 43/1497), S. epidermidis (0.7%, 11/1497) and one S. felis (0.1%, 1/1497). The majority (96.7%, 341/353) of Staphylococcus spp. identified were coagulase-positive (S. pseudintermedius and S. aureus), and only 3.3% (12/353) were coagulase negative (S. epidermidis and S. felis).

While there was an overall increasing temporal trend in both the annual proportion of samples that tested positive for Staphylococcus spp. or S. pseudintermedius during the study period, the proportion of S. aureus positive samples remained stable (Fig. 1).

Based on graphing of the crude proportions of samples that tested positive for Staphylococcus spp., S. aureus and S. pseudintermedius, no seasonal patterns in the distribution of the three variables were apparent (Fig. 2). The very high proportion of Staphylococcus positive samples (100%) and S. pseudintermedius (69.2%) seen in spring of 2010 could be attributed to the small numbers of samples submitted during that season.

Overall, 2012 had the highest proportion of samples that were positive for S. pseudintermedius (31.6%) and S. aureus (5.1%). The highest proportion of S. pseudintermedius positive samples were in Autumn (21.1%) and Spring (21.3%), while the highest proportion of S. aureus positive samples were in Summer (4.8%) (Table 1).

S. pseudintermedius was most common in 2–4 year old dogs (25.6%) followed by dogs in the 7–8 year age category (23.6%). On the other hand, S. aureus was most common in dogs 5–6 years old (6.3%) followed by dogs 2–4 years old (5.3%). Male dogs had the highest proportion of samples that tested positive for S. pseudintermedius (21.0%), while females had the highest proportion of samples that tested positive for S. aureus (4.3%) (Table 1).

Overall, non-sporting breeds had the highest proportion (29.5%) of samples positive for S. pseudintermedius followed by terriers (26.6%). By contrast, crossbreeds had the highest proportion (5.6%) of samples that tested positive for S. aureus followed by herding breeds (5.1%) (Table 1).

S. pseudintermedius and S. aureus were commonly isolated from both skin and ear samples, while abscesses and bone samples did not yield any S. aureus (Fig. 3).

Discussion

This study was designed to assess the burdens and predictors of staphylococcal infections in dogs presented at an academic veterinary hospital in South Africa between 2007 and 2012. We used multinomial logistic regression models to investigate predictors of staphylococcal infections to assess if there were significant differences in predictors across species or if the strength of association differed. Therefore, the results of this study contribute significantly to improving our understanding of the epidemiology of staphylococcal bacterial infections in dogs presented at an academic veterinary hospital in South Africa.

Our results show that Staphylococcus bacteria were isolated from 26.5% of samples submitted to the academic veterinary hospital. This is lower than the 55.1% reported by Wedley et al. (2014) in mainland United Kingdom (UK) and 67.7% by Lilenbaum et al. (2000) in Brazil. The low proportion of Staphylococcus positive samples identified in this study compared to the above mentioned studies may be due to differences in target populations. In this study, we assessed staphylococcal infections among clinical cases of hospitalized dogs, whereas, Wedley et al. (2014) assessed infections in outpatient dogs and Lilenbaum et al. (2000) specifically investigated infection in dogs with otitis.

The significant increasing annual trend in the proportion of Staphylococcus pseudintermedius infections has not been previously reported/investigated in other dog populations. However, this could be attributed to increased access to veterinary services in South Africa since the dawn of democratic South Africa. This would especially be true if there is systematic access to and utilization of veterinary services such that dogs that potentially have high Staphylococcus infection risks are more likely to be presented for diagnostic services at the academic veterinary hospital compared to those with lower staphylococcal infection risks. It is also possible that the increase in the proportions of staphylococcal related infections in this study may be due to progressive poor health and wellbeing of dogs living in and around the area which makes them susceptible to staphylococcal infections. Furthermore, changes in referral practices by surrounding veterinary clinics, changes in owner attitudes towards seeking treatment for chronic skin conditions, and/or changes in lab procedures could have resulted in the increased identification of these infections. Evidence from the current study showed no seasonal pattern in the risk of canine S. pseudintermedius or S. aureus infection. This contrasts with reports of seasonal atopic dermatitis with secondary staphylococcal infections that has been reported by other authors (Simou et al., 2005).

Our study found that Coagulase-Positive Staphylococcus (CoPS) organisms were more common than Coagulase-Negative Staphylococcus (CoNS). This is consistent with the findings by Wedley et al. (2014) who reported higher proportions of CoPS (38%) in dogs compared to CoNS (19%) in the UK. In contrast, Schmidt et al. (2014), in a UK study and Lilenbaum et al. (2000) in a Brazilian study reported a higher frequency of CoNS (95% and 61%) than CoPS (41% and 39%) in dogs. However, it should be noted that in contrast to our study, Schmidt et al. (2014) tested samples collected from healthy Labrador Retrievers. These could explain the differences in the proportions of dogs with CoPS and CoNS infections in the two studies.

S. pseudintermedius was more commonly isolated (19.0%) than S. aureus in this study. However, the observed proportion was lower than 87% reported in Switzerland (Gandolfi-Decristophoris et al., 2013) and 69% reported in Denmark (Paul et al., 2012). Although the prevalence of S. pseudintermedius was higher than that of S. aureus, there was no significant difference between the two species in terms of their affinity for different sample types. Nonetheless, a higher proportion of S. pseudintermedius infections was observed from skin (34.1%) and ear (31.0%) samples compared to other sites/specimens. This is not unexpected because previous studies have reported higher frequency of S. pseudintermedius in dogs with pyoderma or otitis (Wedley et al., 2014; Griffeth et al., 2008; Lilenbaum et al., 2000). These findings can be explained by the fact that S. pseudintermedius is known to be more adapted to colonise the skin surface of dogs than S. aureus (Gandolfi-Decristophoris et al., 2013; Schmidt et al., 2014; Kawakami et al., 2010). Moreover, increased adherence by S. pseudintermedius to corneocytes of canines with atopic dermatitis has been previously reported (McEwan, Mellor & Kalna, 2006) suggesting that dogs are more likely to be infected with S. pseudintermedius compared to other species. Additionally, the results of the study show that ear canal and skin sites compared to other sites are more likely to test positive for S. pseudintermedius or S. aureus than test negative. This further supports research that reports that skin and ear canal compared to other body sites are more likely to be infected with Staphylococcus organism than other bacterial organisms (Gandolfi-Decristophoris et al., 2013; Schmidt et al., 2014; Kawakami et al., 2010).

The high frequency of S. pseudintermedius in dogs visiting the academic veterinary hospital is of public health significance because of association between S. pseudintermedius colonization in dogs and infection in humans with a history of exposure to carrier dogs (Hanselman et al., 2009). Since S. pseudintermedius is not a commensal in the nasal passages of healthy humans, dogs are thought to be an important reservoir for human infections with this pathogen (Tanner et al., 2000).

Although the results of the descriptive analysis indicated that female dogs carried more S. aureus, the results from the multinomial logistic regression indicated that sex of the dog was not a significant predictor of staphylococcal infections in dogs presented at the academic veterinary hospital in South Africa. This is consistent with the findings by Hanselman et al. (2009) who reported no significant association between sex and staphylococcal infections in dogs in Canada. However, our findings are in contrast to findings by Boost, O’Donoghue & James (2008), who reported that female dogs in Japan were more likely to be infected with S. aureus compared to their male counterparts.

The significant association between age and the risk of Staphylococcus infection in dogs observed in the present study was anticipated because age has previously been described as a predictor for Staphylococcus infection in dogs (Boost, O’Donoghue & James, 2008). However, unlike the study by Boost, O’Donoghue & James (2008) that reported more colonization in older dogs compared to puppies and middle aged dogs, in this study dogs ≤6 years of age and 2–6 years of age compared to dogs >8 years of age had a significantly higher risk of S. aureus and S. pseudintermedius infection, respectively, compared to testing negative. It was also noted that the risk of S. pseudintermedius infection was significantly higher in 2–4 year old dogs compared to dogs <2 years of age.

The external validity of this study should be interpreted with caution since it is based on submitted laboratory samples. Moreover, the history of previous use of antibiotics or anti-inflammatory agents was not included in the analysis. It is possible that this could have affected the recovery rates of Staphylococcus species. Since the population under study did not include outpatient cases, the study population should not be regarded as representative of the dog population in Gauteng or of those visiting the teaching hospital. Nonetheless, the results provide a useful preliminary indication of the burden and predictors of staphylococcal infections in dogs presented to the academic veterinary hospital.

Conclusions

This study confirmed that skin, ear and urinary tract infections in dogs presented at the academic veterinary hospital are mainly due to S. pseudintermedius followed by S. aureus. Furthermore, the risk of infection with S. aureus or S. pseudintermedius in dogs presented at the academic veterinary hospital differed by age, with dogs ≤8 years of age often being at higher risk of infection compared to those >8 years old. This is useful information to guide clinical decisions and future studies.