Factors associated with methicillin-resistant versus methicillin-susceptible Staphylococcus pseudintermedius infection in dogs

J. Scott Weese Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada.

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Meredith C. Faires Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada.

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Linda A. Frank Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996.

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Lisa M. Reynolds Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996.

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Antonio Battisti Istituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana, Via Appia Nuova 1411, 00178 Rome, Italy.

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Abstract

Objective—To compare methicillin-resistant Staphylococcus pseudintermedius (MRSP) and methicillin-susceptible S pseudintermedius (MSSP) infections in dogs.

Design—Multicenter case-control study.

Animals—Dogs with MRSP infections were matched, by hospital, with 2 MSSP controls, with the infections occurring immediately before and after the case infection.

Procedures—Signalment, historical, clinical, treatment, and outcome data were documented. Conditional logistic regression was performed. A manual stepwise backward elimination procedure was used to build the multivariable model.

Results—56 case and 112 control dogs were enrolled. Pyoderma was the most common infection type in both groups. In the final multivariable model, systemic administration of antimicrobials within 30 days prior to infection was significantly associated with an MRSP versus an MSSP infection (OR, 9.9; 95% confidence interval, 3.59 to 27.53).

Conclusions and Clinical Relevance—The association of prior antimicrobial administration and MRSP infection indicated the potential impact of routine antimicrobial use in veterinary medicine on antimicrobial resistance and the need for prudent use of these important drugs. Mortality rate was not significantly different between MRSP and MSSP infections; the lack of a significant difference suggested that MRSP was inherently no more virulent than MSSP, provided the infection was properly diagnosed and appropriate treatment was started. Basic concepts such as prudent antimicrobial use and early diagnosis through timely submission of appropriate culture specimens therefore can be important measures to try to reduce the impact of this pathogen.

Abstract

Objective—To compare methicillin-resistant Staphylococcus pseudintermedius (MRSP) and methicillin-susceptible S pseudintermedius (MSSP) infections in dogs.

Design—Multicenter case-control study.

Animals—Dogs with MRSP infections were matched, by hospital, with 2 MSSP controls, with the infections occurring immediately before and after the case infection.

Procedures—Signalment, historical, clinical, treatment, and outcome data were documented. Conditional logistic regression was performed. A manual stepwise backward elimination procedure was used to build the multivariable model.

Results—56 case and 112 control dogs were enrolled. Pyoderma was the most common infection type in both groups. In the final multivariable model, systemic administration of antimicrobials within 30 days prior to infection was significantly associated with an MRSP versus an MSSP infection (OR, 9.9; 95% confidence interval, 3.59 to 27.53).

Conclusions and Clinical Relevance—The association of prior antimicrobial administration and MRSP infection indicated the potential impact of routine antimicrobial use in veterinary medicine on antimicrobial resistance and the need for prudent use of these important drugs. Mortality rate was not significantly different between MRSP and MSSP infections; the lack of a significant difference suggested that MRSP was inherently no more virulent than MSSP, provided the infection was properly diagnosed and appropriate treatment was started. Basic concepts such as prudent antimicrobial use and early diagnosis through timely submission of appropriate culture specimens therefore can be important measures to try to reduce the impact of this pathogen.

Staphylococci are important opportunistic pathogens in many animal species, including dogs. Traditionally, Staphylococcus intermedius has been considered the main staphylococcal pathogen in dogs,1,2 but molecular studies3,4 have recently demonstrated that the closely related organism Staphylococcus pseudintermedius is actually the predominant staphylococcal pathogen in dogs. Regardless of nomenclature, S pseudintermedius infections are a common problem in dogs. Various opportunistic infections can occur; however, skin and ear infections tend to predominate.4–6 Recently, MRSP has emerged as an important problem in dogs internationally, particularly among skin, ear, wound, and surgical site infections.4,7–9 There are numerous and continually increasing reports of MRSP infections in dogs. Two recent studies4,7 have described 103 and 111 MRSP isolates from dogs from North America and Europe and provided insight into the molecular epidemiology of this organism. Colonization of healthy dogs with MRSP may be increasing, considering that recent studies10,11 have reported colonization rates of 4.5% to 5%. These and other studies indicate the importance of this opportunistic pathogen, but they have been unable to evaluate risk factors for MRSP infection or compare MRSP infections with those caused by MSSP. This information is critical for a better understanding of the emergence, dissemination, and clinical relevance of this pathogen of concern. The objective of the study reported here was to compare MRSP and MSSP infections in dogs.

Materials and Methods

A retrospective case-control study was conducted comparing MRSP and MSSP infections in dogs. Three veterinary referral hospitals (OVCTH, UTKCVM, and IZSLT) participated. Cases and controls provided by the OVCTH and UTKCVM were from animals evaluated at those institutions, whereas cases and controls from IZSLT were from private veterinary hospitals. Each hospital identified MRSP and MSSP infections in dogs from June 2007 to October 2009 via the hospital's medical record or microbiology laboratory database. At the time of study enrollment, each case of MRSP infection was matched, by hospital and time, with two control MSSP infections, consisting of the MSSP infection identified immediately preceding the MRSP case and the MSSP infection immediately following the MRSP case. Only animals with clinical infections attributed to S pseudintermedius were included. If the animal was considered to be colonized, on the basis of isolation of S pseudintermedius from a typical colonization site (eg, nares) and a lack of clinical signs of infection, it was excluded.

A pretested standardized questionnairea was used to collect information from the medical records of all cases and controls. Data collected included information on signalment (breed, age, and sex), admission (date of admission and reason for initial evaluation), history (antimicrobial treatment, previous hospitalization, and surgery or medical procedures within 30 days or to date of hospital admission), clinical profile (site of infection, surgery required because of the infection, time of onset of infection with respect to admission, and treatments), and outcome (survival time, duration of hospitalization, and reoccurrence). The infection was classified as CA if it was present at the time of admission or identified within 48 hours after admission, HA-CO if the infection was present at the time of admission but the dog had been hospitalized within 30 days before the onset of infection, and HA if the infection was identified during hospitalization and > 48 hours after admission. Infections were classified as indeterminate if there was inadequate historical or disease-onset information to make a proper assessment. Infections were classified as recurrent if there were 2 or more incidents of infection within a 1-year period.

All descriptive statistics, model building, and analyses were performed with statistical software.b The data set was assessed for missing observations, and any variables that had ≥ 20% of the observations missing were removed prior to analysis. To avoid problems associated with collinearity, a Spearman rank correlation coefficient was performed to investigate pairs of predictor variables, with multiple categories, that had high collinearity with absolute value of r ≥ 0.8. If 2 variables were highly correlated, only 1 of the predictor variables was chosen for use in the model on the basis of biological plausibility and reliability of measurement.12 Analyses were performed by means of conditional logistic regression, with the dependent (outcome) variable defined as dogs having an MRSP or MSSP infection. Information regarding the outcome of the MRSP or MSSP infection was analyzed with descriptive statistics. All tests were 2 sided, and values of P < 0.05 were considered significant.

Univariable analyses were conducted between each predictor variable and the outcome variable with use of a liberal P value of ≤ 0.25. Predictor variables with P > 0.25 were removed prior to construction of the model. Associations between continuous variables and the outcome variable were assessed for linearity graphically by visually assessing whether the log odds of the outcome increased linearly with the predictor variable by use of a lowess smoother12 and by plotting the log odds of the outcome against the predictor after the predictor had been categorized into 5 groups.c If the relationship was not linear, the predictor variable was categorized or modeled with the addition of a quadratic term if appropriate. A manual stepwise backward elimination procedure was used to build the multivariable model. Predictor values were retained in the model if they were significant (P < 0.05). As variables were removed, likelihood ratio tests were used to assess the significance of each model. Strategies to identify confounders and interactions were also used. A variable was deemed a confounder if it changed the coefficient of the predictor variable under investigation by 25% or more. Two-way interactions among all predictor variables in the final model were assessed. Residuals for the final model were also examined. For all predictor variables, ORs and 95% CIs were calculated.

Results

Fifty-six MRSP case and 112 MSSP control dogs were identified and enrolled in this study. Twenty-eight cases were from the UTKCVM, 24 from the OVCTH, and 4 from IZSLT. Signalment data for case dogs and controls were summarized (Table 1). Fifty dog breeds were identified, with mixed breeds being the most common (n = 38 [22.6%]), followed by German Shepherd Dogs (13 [7.7%]), Labrador Retrievers (12 [7.1%]), and Bulldogs (10 [6.0%]). Information pertaining to the onset of infection and comorbidities was summarized (Table 2). Duration of hospitalization was not analyzed because > 20% of observations were missing. Infection site and previous medical procedure information were summarized (Table 3). Although pyoderma predominated in both groups, skeletal infections were also common, accounting for 21% of MRSP and 8.0% of MSSP infections (P = 0.11). Among skeletal infections, 8 of 12 MRSP cases and 5 of 9 MSSP cases were surgical-site infections (P = 0.67). Overall, 32% of MRSP (n = 18) and 24% of MSSP (26) infections were classified as recurrent (P = 0.27). Medications administered within 30 days prior to the onset of infection were summarized (Table 4).

Table 1—

Univariable analysis of signalment data for dogs with MRSP and MSSP infections.

SignalmentCases (n = 56)Controls (n = 112)OR (95% CI)P value
Breed
 Small (1–10 kg)12 (21.4)23 (20.5)Referent 
 Medium (10–25 kg)13 (23.2)18 (16.1)1.35 (0.49–3.72)0.56
 Large (> 25 kg)17 (30.4)47 (41.9)0.68 (0.27–1.72)0.42
 Mixed14 (25.0)24 (21.4)1.04 (0.41–2.68)0.93
Age
 < 6 y29 (51.8)51/111 (45.9)Referent 
 ≥ 6 y27 (48.2)60/111 (54.1)0.79 (0.41–1.51)0.47
Sex
 Spayed female16 (28.6)47 (41.9)Referent 
 Castrated male25 (44.6)30 (26.8)2.36 (1.09–5.10)0.03
 Sexually intact female8 (14.3)14 (12.5)1.71 (0.59–4.94)0.32
 Sexually intact male7 (12.5)21 (18.8)0.95 (0.34–2.65)0.92

Case and control dogs provided by the OVCTH and UTKCVM consisted of animals evaluated at those institutions, whereas case and control dogs provided by the IZSLT consisted of animals evaluated at private veterinary hospitals. Each hospital identified MRSP and MSSP infections in dogs from June 2007 to October 2009 using the hospital's medical record or microbiology laboratory database. At the time of study enrollment, each case of MRSP infection was matched, by hospital and time, with 2 control MSSP infections, consisting of the MSSP infection identified immediately preceding the MRSP case and the MSSP infection immediately following the MRSP case. Only animals with clinical infections attributed to Staphylococcus pseudintermedius were included; colonized animals were ineligible. Data are number (%).

Table 2—

Characterization and univariable analysis of onset of MRSP and MSSP infections and comorbidities in the dogs in Table 1.

VariableCases (n = 56)Controls (n = 112)OR (95% CI)P value
Onset of the infection
 CA23 (41.1)75 (66.9)Referent 
 HA6 (10.7)12 (10.7)1.54 (0.49–4.79)0.46
 HA-CO20 (35.7)11 (9.8)6.00 (2.32–15.53)< 0.01
 Indeterminate7 (12.5)14 (12.5)1.41 (0.47–4.24)0.55
Diabetes mellitus
 No56 (100)109 (97.3)Referent 
 Yes03 (2.7) 
Atopy
 No48 (85.7)100 (89.3)Referent 
 Yes8 (14.3)12 (10.7)1.70 (0.49–5.87)0.39
Fleas
 No52 (92.9)108 (96.4)Referent 
 Yes4 (7.1)4 (3.6)3.00 (0.50–17.95)0.23
Food allergy
 No53 (94.6)109 (97.3)Referent 
 Yes3 (5.4)3 (2.7)2.38 (0.38–14.97)0.36
Hyperadrenocorticism
 No53 (94.6)108 (96.4)Referent 
 Yes3 (5.4)4 (3.6)1.50 (0.34–6.70)0.59
Neoplasia
 No53 (94.6)105 (93.8)Referent 
 Yes3 (5.4)7 (6.2)0.84 (0.20–3.49)0.81
Hypothyroidism
 No54 (96.4)102 (91.1)Referent 
 Yes2 (3.6)10 (8.9)0.35 (0.07–1.73)0.19

Data are number (%).

— = Model did not converge.

Table 3—

Univariable analysis of site and medical associations in the 30 days prior to the onset of the MRSP and MSSP infection in the dogs in Table 1.

VariableCases (n = 56)Controls (n = 112)OR (95% CI)P value
Site of infection
 Skin35 (62.5)59 (52.7)Referent 
 Ears4 (7.1)11 (9.8)0.68 (0.19–2.37)0.55
 Skeletal*12 (21.4)9 (8.0)2.24 (0.83–6.04)0.11
 Urine3 (5.4)17 (15.2)0.26 (0.06–1.03)0.05
 Other2 (3.6)16 (14.3)0.17 (0.03–0.89)0.04
Hospitalized
 No31 (55.4)91 (81.3)Referent 
 Yes25 (44.6)21 (18.7)3.47 (1.67–7.21)< 0.01
Outpatient visit
 No20 (37.7)54 (51.4)Referent 
 Yes33 (62.3)51 (48.6)1.71 (0.82–3.56)0.15
Surgery
 No33 (60)92 (82.1)Referent 
 Yes22 (40)20 (17.9)3.16 (1.46–6.86)< 0.01
Urinary catheterization
 No55 (98.2)109 (99.1)Referent 
 Yes1 (1.8)1 (0.9)2.00 (0.13–31.98)0.62

Data are number (%).

Includes bone and joint fluid.

Includes eyes, vagina, uterus, trachea, mouth, blood, and body cavity (fluid).

For outpatient visits, n = 53 for cases and 105 for controls. For surgery, n = 55 for cases. For urinary catheterization, n = 110 for controls.

Table 4—

Univariable analysis of medications given within 30 days prior to the onset of the MRSP and MSSP infection in the dogs in Table 1.

VariableCasesControlsOR (95% CI)P value
Received systemic antimicrobials
 No13/54 (24.1)72/111 (64.9)Referent 
 Yes41/54 (75.9)39/111 (35.1)8.55 (3.27–22.34)< 0.01
No. of antimicrobial classes prescribed
 013/52 (25)72/106 (67.9)Referent 
 132/52 (61.5)26/106 (24.5)8.38 (3.18–22.10)< 0.01
 27/52 (13.5)8/106 (7.5)8.91 (2.23–35.61)< 0.01
Received a β-lactam
 No20/52 (38.5)79/106 (74.5)Referent 
 Yes32/52 (61.5)27/106 (25.5)4.26 (2.03–8.92)< 0.01
Received chloramphenicol
 No48/52 (92.3)106/106 (100)Referent 
 Yes4/52 (7.7)0 
Received a fluoroquinolone
 No48/52 (92.3)98/106 (92.5)Referent 
 Yes4/52 (7.7)8/106 (7.6)1.00 (0.29–3.50)1.00
Received a lincosamide
 No48/52 (92.3)104/106 (98.1)Referent 
 Yes4/52 (7.7)2/106 (1.9)5.77 (0.62–53.60)0.123
Received trimethoprim-sulfamethoxazole
 No51/52 (98.1)104/106 (98.1)Referent 
 Yes1/52 (1.9)2/106 (1.9)1.00 (0.09–11.03)1.00
Received a tetracycline
 No51/52 (98.1)106/106 (100)Referent 
 Yes1/52 (1.9)0 
Received local antimicrobials
 No44/55 (80)96/111 (86.5)Referent 
 Yes11/55 (20)15/111 (13.5)2.00 (0.68–5.88)0.21
Received corticosteroids
 No48/55 (87.3)90/112 (80.4)Referent 
 Yes7/55 (12.7)22/112 (19.6)0.54 (0.20–1.45)0.22
Received immunosuppressive treatment
 No52/56 (92.9)101/111 (91.0)Referent 
 Yes4/56 (7.1)10/111 (9.1)0.79 (0.24–2.61)0.69

Data are No. in category/total No. of dogs (%).

— = Dropped because of all positive or all negative outcomes.

In the final multivariable model (Table 5), systemic administration of antimicrobials was significantly (P < 0.01) associated with an MRSP versus an MSSP infection, with an OR of 9.9 (95% CI, 3.6 to 27). Being a castrated male, compared with being a spayed female, was significantly (P = 0.02) associated with an MRSP infection (OR, 3.01; 95% CI, 1.15 to 7.84). Results from the contrasts created among the categories of the predictor variable sex indicated that castrated males versus sexually intact females (OR, 1.09; 95% CI, 0.29 to 4.10; P = 0.90), castrated males versus sexually intact males (OR, 2.39; 95% CI, 0.67 to 8.45; P = 0.18), and sexually intact females versus sexually intact males (OR, 2.19; 95% CI, 0.45 to 10.6; P = 0.33) were not significantly different. No confounders or interactions were identified. Three observations were identified with large residuals and investigated; however, no recording error was detected, and the observations were retained in the data set.

Table 5—

Variables significantly associated with MRSP infection, compared with MSSP infection, in dogs (n = 168) in the final multivariable model.

VariableOR (95% CI)P value
Sex
 Spayed femaleReferent 
 Castrated male3.01 (1.15–7.84)0.02
 Sexually intact female2.76 (0.73–10.49)0.14
 Sexually intact male1.26 (0.36–4.45)0.72
Systemic antimicrobials
 NoReferent 
 Yes9.94 (3.59–27.53)< 0.01

There was no difference in mortality rates (P = 0.61), with death or euthanasia occurring in 10.7% of MRSP (n = 6) case animals and 6.3% of MSSP (7) controls. The outcome for 16.1% of MRSP case animals (n = 9) and 18.7% of MSSP (21) controls was not known. Of the animals that died or were euthanized, death was attributed to S pseudintermedius infection in only 2 of 6 MRSP case animals and 3 of 7 MSSP controls.

Discussion

In the present study, there was a significant association between recent (within 30 days) prior antimicrobial administration and MRSP infection in dogs. Methicillin-resistant S pseudintermedius infections are an emerging and potentially serious problem in small animal medicine. The apparent speed with which MRSP has emerged internationally and the highly drug-resistant nature of many isolates have caused tremendous concern.d Identification of associations and characterization of MRSP infections are important to help elucidate the epidemiology of MRSP infections, to identify possible ways to reduce infections, and to provide better clinical guidance for management of infections and counseling owners of affected animals.

Pyoderma and otitis accounted for the majority of MRSP (69.6%) and MSSP (62.5%) infections in the present study, a finding that is not unexpected given the known predominance of S pseudintermedius in these 2 conditions.13,14 There is currently no evidence that MRSP is more invasive or able to cause different types of disease than MSSP, so it was expected that infection types and sites would be similar for MRSP and MSSP.

Orthopedic infections were common in this study, and although there was not a significant difference in musculoskeletal infections between the 2 groups, the high number of MRSP orthopedic infections (including surgical-site infections) is of concern because of the potential difficulty treating many of these infections. In particular, anecdotal evidence suggests that surgical-site infections after tibial plateau leveling osteotomy are a major concern and an increasingly common type of infection.

The association of MRSP with castrated males (compared with spayed females) in both the univariable and multivariable analyses was interesting and defies ready explanation. Determination of origin of infection is difficult retrospectively, and although guidelines are in place for classification of suspected origin of infection,15 these are far from definitive. The criteria used in this study permitted classification of infections as CA, HA, and HA-CO. Inclusion of the HA-CO group is important because infections acquired during hospitalization are not always identified by the time of discharge, particularly in cases where duration of hospitalization is short. The overrepresentation of HA-CO infections among MRSP infections in the univariable analysis may indicate an impact of hospitalization on MRSP infection. This could be from acquisition of the organism in hospitals but could also represent increased likelihood of infection from the animals' own microflora because of exposure to other possible risk factors (eg, antimicrobial administration) during hospitalization. The main concern about such classification and analysis is the empirical nature of the criteria and the inability to definitely determine origin of infection. Regardless, this type of classification provides useful information for development of further studies investigating the origin of infections.

On the basis of the univariable analysis, surgery was significantly associated with an MRSP infection in this study. An association between surgery and MRSP infection would not be surprising, given increasing reports of postoperative MRSP infections and the resistance of MRSP to commonly used perioperative antimicrobials. However, neither hospitalization nor surgery was identified as a risk factor in the multivariable model. Although there may be no true association, this could also be a function of sample size and statistical power, so further focused study of the role of hospitalization and surgery on the risk of MRSP infection is required.

The association between antimicrobial exposure within 30 days and MRSP infection in the present study was unsurprising but is important to document. This result is similar to 2 recent studies comparing MRSA and MSSA infection in dogs; one identified administration of β-lactam antimicrobials or fluoroquinolones within the previous 90 days as associated with MRSA versus MSSA infection,16 and the other reported the number of antimicrobial courses as a risk factor.17 These 2 reports16,17 as well as our results provide further impetus to develop and implement prudent antimicrobial use practices in veterinary medicine. Although elimination of MRSP is not a realistic goal, measures that could reduce the likelihood of a resistant versus susceptible infection are critical, given the importance of this pathogen in animal health.

Mortality rates were reasonably low for both groups (10.7% among MRSP case dogs and 6.3% among MSSP case dogs), and there was no significant difference between groups. This is consistent with results of a similar study16 of MRSA versus MSSA infections in dogs and provides further support to the notion that methicillin-resistant staphylococcal infections are not inherently more virulent than their methicillin-susceptible counterparts. However, a few factors must be considered. First, enrollment in this study required a diagnosis, and diagnosis of MRSP would hopefully lead to initiation of appropriate targeted antimicrobial treatment. If specimens are not submitted for culture and MRSP is not identified, the outcome for patients with MRSP infections could be worse than those with MSSP infections because of the resistance of MRSP to most antimicrobials that are used empirically. Second, studies such as this have an inherent risk of underreporting mortality rates because it is possible that some animals could have died or been euthanized in other veterinary clinics without the knowledge of the participating clinics or veterinarians. Finally, most infections in the present study were noninvasive infections (ie, ear, skin, and bladder infections) that are unlikely to be fatal. Study of larger numbers of patients with invasive infections would be useful to more specifically evaluate the potential impact on survival time.

As with most retrospective studies, there are potential limitations on the basis of the quality of data in the medical record. However, there is no reason to suspect that errors or deficiencies in medical record data would differ between MRSP and MSSP cases. Another aspect that bears consideration is the method for identification of MRSP. Recently, Clinical and Laboratory Standards Institute guidelines for detection of methicillin-resistance in S pseudintermedius have been changed18 because of recognition that previously used methods might have resulted in misclassification of MRSP as MSSP. It is unclear whether there may have been some misclassified isolates in this data set. If such a misclassification occurred, it is reasonable to assume that the most likely effect would be to decrease the chance of identifying significant differences between MRSP and MSSP (by virtue of having some cases in the control group), rather than leading to erroneous associations. The use of a matched-pairs analysis also precludes investigation of the effect of facility or time of year. However, matching by hospital and time was performed because both are potential confounding variables. Further, these types of data can indicate associations between MRSP infection and specific variables but not necessarily indicate a causal relationship.

The emergence and dissemination of MRSP in dogs have caused tremendous concern because of the high-profile nature of methicillin resistance, the concurrent resistance of MRSP isolates to other antimicrobial classes, the apparently rapid increase in incidence and prevalence of MRSP in dogs, and the considerable impact of MRSA in human medicine. Although the reasons for the spread of this pathogen require further investigation, the results of the present study indicate that factors such as antimicrobial treatment play an important role in the epidemiology of MRSP in dogs. Other factors such as hospitalization and surgical procedures may also be important. Although these factors are not completely avoidable, identification of their possible role in driving MRSP infections is further evidence of the need for prudent antimicrobial use, along with development and implementation of good, routine infection-control practices in veterinary hospitals.

ABBREVIATIONS

CA

Community associated

CI

Confidence interval

HA

Hospital associated

HA-CO

Hospital associated, community onset

IZSLT

Veterinary Institute of Latium and Tuscany, Central Italy

MRSA

Methicillin-resistant Staphylococcus aureus

MRSP

Methicillin-resistant Staphylococcus pseudintermedius

MSSA

Methicillin-susceptible Staphylococcus aureus

MSSP

Methicillin-susceptible Staphylococcus pseudintermedius

OVCTH

Ontario Veterinary College Veterinary Teaching Hospital

UTKCVM

University of Tennessee, Knoxville, College of Veterinary Medicine

a.

Questionnaire available upon request.

b.

Stata, version 10.0, StataCorp, College Station, Tex.

c.

Lintrend, Stata, version 10.0, StataCorp, College Station, Tex.

d.

Gronlund-Andersson U, Finn M, Kadlec K, et al. Methicillin-resistant Staphylococcus pseudintermedius: an emerging companion animal health problem (abstr), in Proceedings. Am Soc Microbiol Eur Soc Clin Microbiol Infect Dis Conf Methicillin Resist Staphylococci Anim 2009;A-40.

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