Prevalence and antimicrobial resistance of Enterococcus spp and Staphylococcus spp isolated from surfaces in a veterinary teaching hospital

Elizabeth Hamilton Center for Comparative Epidemiology, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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John B. Kaneene Center for Comparative Epidemiology, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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Katherine J. May Center for Comparative Epidemiology, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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John M. Kruger Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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William Schall Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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Matthew W. Beal Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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Joe G. Hauptman Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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Charles E. DeCamp Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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Abstract

Objective—To determine the prevalence and antimicrobial resistance of enterococci and staphylococci collected from environmental surfaces at a veterinary teaching hospital (VTH).

Design—Longitudinal study.

Sample—Samples collected from surfaces in 5 areas (emergency and critical care, soft tissue and internal medicine, and orthopedic wards; surgery preparation and recovery rooms; and surgery office and operating rooms) of a VTH.

Procedures—Selected surfaces were swabbed every 3 months during the 3-year study period (2007 to 2009). Isolates of enterococci and staphylococci were identified via biochemical tests, and antimicrobial susceptibility was evaluated with a microbroth dilution technique. A subset of isolates was analyzed to assess clonality by use of pulsed-field gel electrophoresis.

Results—430 samples were collected, and isolates of enterococci (n = 75) and staphylococci (110) were identified. Surfaces significantly associated with isolation of Enterococcus spp and Staphylococcus spp included cages and a weight scale. Fourteen Enterococcus spp isolates and 17 Staphylococcus spp isolates were resistant to ≥ 5 antimicrobials. Samples collected from the scale throughout the study suggested an overall increase in antimicrobial resistance of Enterococcus faecium over time. Clonality was detected for E faecium isolates collected from 2 different surfaces on the same day.

Conclusions and Clinical Relevance—Although not surprising, the apparent increase in antimicrobial resistance of E faecium was of concern because of the organism's ability to transmit antimicrobial resistance genes to other pathogens. Results reported here may aid in identification of critical control points to help prevent the spread of pathogens in VTHs.

Abstract

Objective—To determine the prevalence and antimicrobial resistance of enterococci and staphylococci collected from environmental surfaces at a veterinary teaching hospital (VTH).

Design—Longitudinal study.

Sample—Samples collected from surfaces in 5 areas (emergency and critical care, soft tissue and internal medicine, and orthopedic wards; surgery preparation and recovery rooms; and surgery office and operating rooms) of a VTH.

Procedures—Selected surfaces were swabbed every 3 months during the 3-year study period (2007 to 2009). Isolates of enterococci and staphylococci were identified via biochemical tests, and antimicrobial susceptibility was evaluated with a microbroth dilution technique. A subset of isolates was analyzed to assess clonality by use of pulsed-field gel electrophoresis.

Results—430 samples were collected, and isolates of enterococci (n = 75) and staphylococci (110) were identified. Surfaces significantly associated with isolation of Enterococcus spp and Staphylococcus spp included cages and a weight scale. Fourteen Enterococcus spp isolates and 17 Staphylococcus spp isolates were resistant to ≥ 5 antimicrobials. Samples collected from the scale throughout the study suggested an overall increase in antimicrobial resistance of Enterococcus faecium over time. Clonality was detected for E faecium isolates collected from 2 different surfaces on the same day.

Conclusions and Clinical Relevance—Although not surprising, the apparent increase in antimicrobial resistance of E faecium was of concern because of the organism's ability to transmit antimicrobial resistance genes to other pathogens. Results reported here may aid in identification of critical control points to help prevent the spread of pathogens in VTHs.

Companion animals play an important role in the transmission of antimicrobial-resistant bacteria to humans and other animals.1–5 Bacteria typically found in dogs, such as Staphylococcus pseudintermedius, have the ability to carry and transfer antimicrobial resistance genes to other pathogenic bacteria,6 and the hospital environment can act as a reservoir for drug-resistant pathogens.2,4,7

To date, few studies7–9 have explored the diversity of bacteria present on environmental surfaces within a VTH. Certain objects in a clinical setting can serve as ideal vehicles in the transmission of organisms between humans and animals. There have been previous studies of isolation of pathogenic and nonpathogenic organisms from objects within VTHs, such as treatment tables and cages,7 door handles,8,10 and floors.1

The role of the veterinary hospital environment in transmission of pathogens should be at the forefront of studies regarding health-care–associated infections. As with any hospital or clinical setting, emergence of health-care–associated infections with antimicrobial-resistant bacteria is of concern because many patients are at risk for infection and may return to their home environments carrying antimicrobial-resistant bacteria. Although infection control practices within VTHs have not been widely studied, a recent report8 described application of human-hospital standards for infection control within a VTH. Studies such as these are vital, considering that interactions between health-care providers and patients in VTHs can be quite different from those in human hospitals.

In recent years, substantial evidence has been provided to support the idea that veterinary hospitals play a part in the transmission of antimicrobial-resistant organisms.1,2,5,7,10 Not only do veterinary hospital staff supply and administer antimicrobials, but there are ample opportunities for close interaction between humans and animals. These interactions provide opportunities for the development of antimicrobial resistance and transmission of antimicrobial-resistant organisms. The objective of the study reported here was to determine the prevalence and antimicrobial resistance patterns of Enterococcus spp and Staphylococcus spp collected from environmental surfaces at a VTH during a longitudinal (3-year) study.

Materials and Methods

Study design—A cross-sectional study of samples from selected areas in the Michigan State University VTH was conducted from February 5, 2007, through December 29, 2009. Environmental samples were collected at the beginning of every fourth clinical rotation, which was approximately every 3 months, from the same surfaces and areas throughout the VTH, resulting in 13 rounds of repeated sample collection.

Sample collection—Five areas (ECC, soft tissue and internal medicine, and orthopedic wards; surgery preparation and recovery rooms; and surgery office and operating rooms) in the VTH were chosen for inclusion in the present study. Within each area, the following surfaces were identified for sample collection where applicable: animal cages (including runs; samples were collected from the doors and floors), door handles, examination tables, treatment floor (part of the floor in the ECC where animals lay while being cared for), floor drains, hose ends and connectors, computer keyboards, telephones, leashes, weight scale (1 scale in the soft tissue and internal medicine ward), sinks and sink drains, suction canisters in the clean-up sink, suction and tank control knobs, IV administration set poles, storage cabinet handles, light switches, and water blankets. Not all collection surfaces were present in each area; for example, cages were present in the ECC, soft tissue and internal medicine ward, orthopedic ward, and surgery recovery rooms (samples were collected from 1 occupied cage in each area, and this may not have been the same cage at each sample collection); however, computer keyboards were only present in the orthopedic ward and surgery office.

Samples were collected between 2 pm and 3 pm because patients had typically been examined or treated in the sample collection areas by this time. General surface-specific cleaning was performed as patients were seen; however, more thorough cleaning was performed by janitorial staff after 4 pm each day. Samples were collected with a sterile swab and placed in a transport tube containing Stuart transport medium.a Each sample was collected by running a swab moistened with transport medium over the area of each surface and simultaneously twirling the swab tip. For example, when samples were collected from a keyboard, the swab was run and twirled over all keys of the keyboard. When samples were collected from a cage, the swab was run and twirled over the latching mechanism, the portion of the door that was adjacent to the floor, the opening of the cage, and the front edge of the cage floor. Collected samples were then immediately submitted to the Michigan State University Center for Comparative Epidemiology Microbial Epidemiology Laboratory to be processed.

Isolation and identification of microbes—Swabs were streaked onto individual Columbia colidixin and nalidixic acid agar plates supplemented with 5% sheep blood, incubated for 48 hours at 37°C, and grossly inspected for typical morphology. One to 5 colonies/plate with typical Enterococcus spp and Staphylococcus spp morphology were chosen for identification.

Identification of enterococci was completed with commercially available biochemical test strips for identification of streptococci and related bacteriab in accordance with the manufacturer's instructions, and species identification was performed by use of the test strip manufacturer's database.c Identification of staphylococci was completed by a series of biochemical tests, including inoculation of Pseudomonas agar P, Voges-Proskauer, trehalose, maltose, and urea media. Results of Pseudomonas agar P tests were considered positive if growth of the microorganism was detected. Voges-Proskauer reaction, trehalose and maltose fermentation, and urease test results were interpreted on the basis of the presence (positive) or absence (negative) of detectable color changes. A coagulase test was also performed. Positive results for Pseudomonas agar P, Voges-Proskauer reaction, trehalose and maltose fermentation, urease, and coagulase tests were used to identify Staphylococcus aureus. Negative results for Pseudomonas agar P and Voges-Proskauer reaction tests with positive results for trehalose fermentation and urease tests, positive or negative results for maltose fermentation tests, and mixed coagulase test results were used to identify Staphylococcus intermedius at the start of the study. After the present study was initiated, another study11 was published that provided evidence concerning misclassification of S intermedius. Therefore, these organisms were classified as SIG (including S intermedius, S pseudintermedius, Staphylococcus delphini, Staphylococcus schleiferi subsp coagulans, Staphylococcus hyicus, or Staphylococcus lutrae) rather than as S intermedius.

Any isolates that did not have results typical for S aureus or SIG were then tested further with commercially available test strips for identification of staphylococcid in accordance with the manufacturer's instructions, and species identification was performed by use of the test strip manufacturer's database.e After species identification, these isolates were further grouped as SIG or CoNS (including Staphylococcus epidermidis, Staphylococcus haemolyticus, Staphylococcus hominis, Staphylococcus warneri, Staphylococcus chromogenes, Staphylococcus xylosus, Staphylococcus saprophyticus, Staphylococcus caprae, Staphylococcus cohnii subsp ureolyticus, Staphylococcus sciuri, and Staphylococcus lugdunensis) for purposes of analysis.

One to 5 positively identified isolates of Enterococcus spp or Staphylococcus spp from each sample were individually suspended in tryptic soy broth; 0.5 mL of the suspension was added to 0.5 mL of 65% glycerol solution, and the mixture was frozen at −70°C. Additionally, the isolates were stabbed onto tryptic soy agar and stored at room temperature (approx 22°C) until antimicrobial susceptibility testing was performed.

Antimicrobial susceptibility testing—A microdilution systemf was used to perform antimicrobial susceptibility testing on a commercially prepared plate.g To ensure inclusion of antimicrobials used in both human and animal medicine, ampicillin, oxacillin, penicillin, ceftriaxone, ciprofloxacin, levofloxacin, gatifloxacin, clindamycin, daptomycin, erythromycin, gentamicin, vancomycin, linezolid, quinupristin-dalfopristin, rifampin, tetracycline, and trimethoprim-sulfamethoxazole were used in susceptibility testing. Enterococcus faecalis (ATCC 29212), S aureus (ATCC 29213), and Escherichia coli (ATCC 25922) were used for quality-control purposes. Quality-control results were reviewed for each batch of tests, all of which were within acceptable limits. Inducible clindamycin resistance was not investigated.

The minimum inhibitory concentration value at which no growth occurred was measured with a fluorescence technology-based automated reading system,h and an antimicrobial susceptibility and resistance profile was generated. Susceptibility, intermediate resistance, and resistance were determined by comparison with Clinical and Laboratory Standards Institute breakpoints.12 Enterococcal resistance to gentamicin, ceftriaxone, clindamycin, trimethoprim-sulfamethoxazole, and oxacillin was not interpreted. An isolate was determined to have pentaresistance if it was resistant to ≥ 5 of the antimicrobials tested.

PFGE—To determine relatedness between different isolates of the same species in selected samples, PFGE was performed in a preliminary experiment. Nine isolates (7 Enterococcus faecium and 2 E faecalis) were chosen on the basis of collection site and date to maximize the opportunity for identification of related clones, and PFGE was performed according to Michigan State University Diagnostic Center for Population and Animal Health standard operating procedures. The restriction enzyme SmaI was used, and electrophoresis was performed with a PFGE unit,i ramping the switch times from 4 seconds to 35 seconds. The overall run time was 20 hours. Pulsed-field gel electrophoresis clone groupings were determined according to the standard of Tenover et al.13

Statistical analysis—Because up to 5 typical colonies each of Enterococcus spp and Staphylococcus spp were chosen from each sample, susceptibility patterns produced by applying Clinical and Laboratory Standards Institute breakpoints12 to all antimicrobials tested were compared for each group of species isolated from each surface at each sample collection time to prevent unnecessarily overcounting the organisms. Any species with identical susceptibility patterns, sample collection dates, and sample collection surfaces were restricted, and 1 isolate was randomly chosen for inclusion in the analysis.

The proportion of organisms recovered by surface and area were calculated and compared by use of a commercially available statistical software program.j A Fisher exact test (2 tailed) was performed to compare the proportion of organisms recovered from each surface and area with that of all other surfaces and areas for that organism. Univariate (χ2) analysis was performed for the independent variables of surface and area. These categorical variables were transformed into dummy variables for analysis. For surface, the dummy variables were cages, examination tables, the treatment floor, floor drains, keyboards, telephones, the scale, and all other surfaces, with door handle selected as the referent category. For area, the dummy variables were ECC ward, soft tissue and internal medicine ward, orthopedic ward, and surgery office and operating rooms, with surgery preparation and recovery rooms selected as the referent category. Both independent variables (surface and area) had a value of P < 0.2 and were included in 2 multivariate logistic regression models, with isolation of enterococci or staphylococci as the outcome variable. Odds ratios and 95% CIs were reported, and associations were considered significant if the 95% CI did not include 1.0.

For analysis of antimicrobial susceptibility, the proportion of species isolated, along with the proportions of antimicrobial resistant and pentaresistant organisms, was calculated. The MIC50 and MIC90 were determined for selected surfaces and antimicrobials. Antimicrobials for comparison were chosen on the basis of clinical importance or to evaluate variability in resistance among different species of bacteria. Finally, the MIC50 of all antimicrobials tested was determined for isolates repeatedly recovered from the scale at the various sample collection times throughout the study to evaluate changes in resistance over time.

Results

Prevalence of enterococci and staphylococci—A total of 430 samples from surfaces throughout the VTH were collected. Of these, Enterococcus spp were isolated from 41 samples and Staphylococcus spp were isolated from 68 samples (Table 1). Bacteria were isolated from all sample collection areas throughout the VTH; however, not all surfaces within those areas were contaminated. Enterococci and staphylococci were not isolated from sinks or sink drains.

Table 1—

Summary of 430 samples collected and Enterococcus spp (n = 41 samples) and Staphylococcus spp (68) isolated from selected surfaces and areas of a VTH from February 5, 2007, to December 29, 2009.

VariableAll samples*Enterococcus sppStaphylococcus spp
No.Total samples (%)No.Total surface or area (%)P valueNo.Total surface or area (%)P value
Surface
 Cages6615.31319.70.0021624.20.041
 Treatment floor133.0430.80.027646.20.002
 Door handles399.137.71.025.10.064
 Examination tables153.50640.00.009
 Floor drains266.0311.50.72713.80.099
 Keyboards266.0519.20.082934.60.007
 Leashes133.017.71.0323.10.442
 Telephones6515.169.20.9281218.50.525
 Scale133.0538.5< 0.001969.2< 0.001
 Sink and sink drains5212.100
 Surgery preparation items419.5012.40.011
 Surgery operating room items6114.211.60.01834.90.012
Area
 Soft tissue and internal medicine ward7918.41417.70.0062531.6< 0.001
 ECC ward6515.11015.40.0811015.40.918
 Orthopedic ward9121.21213.20.1821516.50.844
 Surgery preparation and recovery rooms7317.034.10.12368.20.051
 Surgery office and operating rooms12228.421.6< 0.001129.80.033

Association of surface or area with isolation of Enterococcus spp or Staphylococcus spp was assessed by means of χ2 and Fisher exact (for cells with counts < 5) tests. Suction canisters were combined with sink and sink drains because samples were collected while in the clean-up sink. Surgery preparation items included sterilized capnograph connectors, hose ends, and intravenous poles. Surgery operating room items included wall light switches, cabinet handles, water blankets, and control knobs within a surgical suite.

Samples were collected from selected surfaces and areas at the beginning of every fourth clinical rotation (approx every 3 months) for a total of 13 time points. Not all surfaces were present in all areas.

Number of samples from which the species of interest was isolated.

— = Not applicable.

The soft tissue and internal medicine ward had the highest percentages of Enterococcus spp (14/79 [17.7%] samples) and Staphylococcus spp (25/79 [31.6%]) isolated, and the surgery operating rooms and offices had the lowest and second lowest percentages (2/122 [1.6%] and 12/122 [9.8%] for Enterococcus spp and Staphylococcus spp, respectively). These were the only 2 areas significantly associated with the isolation of Enterococcus spp and Staphylococcus spp when evaluated by means of χ2 and Fisher exact tests (Table 1).

Surfaces with the highest proportion of Enterococcus spp were the treatment floor (4/13 samples) and scale (5/13), and surfaces with the highest proportion of Staphylococcus spp were the treatment floor (6/13 samples), examination tables (6/15), and scale (9/13; Table 1). Results of univariate analysis for the variable of surface (with door handle as the referent category) revealed that cages, treatment floor, and scale were significantly associated with isolation of Enterococcus spp (Table 2). However, isolation of Staphylococcus spp was significantly associated with all surfaces except for telephones, floor drains, and surfaces designated as other. Notably, the likelihood of isolating either organism from the scale was quite high for enterococci (OR, 10.625; 95% CI, 2.116 to 53.356) and staphylococci (OR, 41.625; 95% CI, 6.564 to 263.957). Univariate analysis of area (with surgery preparation and recovery rooms as the referent category) revealed that the soft tissue and internal medicine ward (OR, 5.026; 95% CI, 1.381 to 18.291) and ECC ward (OR, 4.242; 95% CI, 1.113 to 16.164) areas were significantly associated with isolation of enterococci; however, only the soft tissue and internal medicine ward (OR, 5.17; 95% CI, 1.989 to 13.507) was significantly associated with isolation of staphylococci.

Table 2—

Univariate ORs and 95% CIs for isolation of Enterococcus spp or Staphylococcus spp from selected surfaces and areas of a VTH from February 5, 2007, to December 29, 2009.

VariableEnterococcus sppStaphylococcus spp
OR95% CIP valueOR95% CIP value
Surface
 Door handlesRef< 0.001Ref< 0.001
 Cages4.171.12–15.50 5.921.28–27.35 
 Examination tables 12.332.13–71.57 
 Treatment floor7.561.44–39.59 15.862.64–95.23 
 Floor drains2.220.42–11.83 0.740.06–8.61 
 Keyboards4.050.89–18.49 9.791.91–50.30 
 Telephones1.730.41–7.27 4.190.89–19.83 
 Scale10.6252.116–53.356 41.6256.564–263.957 
 Other0.2060.034–1.267 0.8090.162–4.056 
Area
 Surgery preparation and recovery roomsRef< 0.001Ref< 0.001
 Surgery operating room and office0.3890.063–2.384 1.2180.437–3.398 
 Soft tissue and internal medicine ward5.0261.381–18.291 5.171.989–13.507 
 ECC ward4.2421.113–16.164 2.030.694–5.937 
 Orthopedic ward3.5440.961–13.076 2.2040.809–6.003 

Other surfaces included leashes, sinks and sink drains, sterile capnograph connectors, hose ends, intravenous poles, wall light switches, cabinet handles, water blanket, and control knobs within a surgical suite.

Ref = Referent category.

See Table 1 for remainder of key.

When the model was controlled for surface, none of the areas were significantly associated with isolation of either organism (Table 3). Significant associations detected between surfaces and isolation of staphylococci were retained and became more precise. Associations of cages and scale with isolation of enterococci were retained and were more precise; however, the treatment floor was no longer significantly associated with isolation of enterococci, and keyboards were significantly associated with this outcome variable.

Table 3—

Multivariate logistic regression model of risk factors associated with isolation of Enterococcus spp or Staphylococcus spp from the same surfaces and areas in Table 2.

VariableEnterococcus sppStaphylococcus spp
OR95% CIOR95% CI
Surface
 Door handlesRefRef
 Cages3.981.03–14.625.301.09–25.78
 Examination tables9.241.35–63.11
 Treatment floor5.840.96–35.4326.703.54–201.61
 Floor drains2.90.34–12.860.480.04–5.82
 Keyboards6.901.23–38.707.071.28–39.13
 Telephones2.020.48–8.603.800.78–18.64
 Scale8.3281.463–47.39230.7984.024–235.698
 Other0.3950.061–2.5580.7150.13–3.919
Area
 Surgery preparation and recovery roomsRefRef
 Surgery operating room and office0.4190.056–3.1121.4510.453–4.643
 Soft tissue and internal medicine ward2.3350.579–9.4151.5910.521–4.857
 ECC ward2.3680.543–10.3280.6990.18–2.714
 Orthopedic ward1.9310.444–8.3881.8270.608–5.494

See Tables 1 and 2 for key.

Antimicrobial susceptibility testing—Resistance to tested antimicrobials was highly prevalent among Enterococcus spp, and these isolates were most commonly resistant to rifampin (33/75 [44%]) and quinupristin-dalfopristin (34/75 [45%]; Table 4). Nearly all isolates of Enterococcus spp (71/75 [94.7%]) were resistant to ≥ 1 antimicrobial, and 19.7% (14/71) of these had pentaresistance (Table 5).

Table 4—

Results of antimicrobial susceptibility testing for Enterococcus spp (n = 75) and Staphylococcus spp (110) isolated from the same VTH surfaces and areas in Table 1.

Class and antimicrobialInterpretive breakpoints (μg/mL)*Enterococcus sppStaphylococcus spp
SusceptibleResistantNo. susceptibleNo. intermediateNo. (%) resistantNo. susceptibleNo. intermediateNo. (%) resistant
Aminoglycoside
 Gentamicin≤ 4≥ 16NININI9974 (4)
Cephalosporin
 Ceftriaxone≤ 8≥ 32NININI94124 (4)
Fluoroquinolone
 Ciprofloxacin≤ 1≥ 4391719 (25)95411 (10)
 Gatifloxacin≤ 2 (enterococci) and ≤ 0.5 (staphylococci)≥ 8 (enterococci) and ≥ 4 (staphylococci)61311 (15)9773 (66)
 Levofloxacin≤ 2 (enterococci) and ≤ 1 (staphylococci)≥ 8 (enterococci) and ≥ 4 (staphylococci)61113 (17)96113 (12)
Glycopeptide
 Vancomycin≤ 4 (enterococci) and ≤ 2 (staphylococci)≥ 32 (enterococci) and ≥ 16 (staphylococci)723110
Lincosamide
 Clindamycin≤ 0.5≥ 4NININI88814 (13)
Lipopeptide
 Daptomycin≤ 1NA75110
Macrolide
 Erythromycin≤ 0.5≥ 8282621 (28)66440 (36)
Oxazolidinone
 Linezolid≤ 2 (enterococci) and ≤ 4 (staphylococci)NA75110
β-Lactam
 Ampicillin≤ 8 (enterococci) and ≤ 0.25 (staphylococci)≥ 16 (enterococci) and ≥ 0.5 (staphylococci)4629 (39)8327 (25)
 Oxacillin≤ 2 (Staphylococcus aureus and SIG) and ≤ 0.25 (CoNS)≥ 4 (S aureus and SIG) and ≥ 0.5 (CoNS)NININI7436 (33)
 Penicillin≤ 8 (enterococci) and ≤ 0.12 (staphylococci)≥ 16 (enterococci) and ≥ 0.25 (staphylococci)4530 (40)6446 (42)
Rifampin
 Rifampin≤ 1≥ 433933 (44)1091
Streptogramin
 Quinupristin-dalfopristin≤ 1≥ 4172434 (45)1091
 Sulfonamide Trimethoprim-sulfamethoxazole≤ 2/38≥ 4/76NININI1073 (3)
Tetracycline
 Tetracycline≤ 4≥ 1638532 (43)93116 (15)

Susceptibility, intermediate resistance, and resistance were determined by comparison with Clinical and Laboratory Standards Institute breakpoints.12

NA = Interpretive breakpoint for resistance was not available. NI = Minimum inhibitory concentrations of these antimicrobials were not interpreted.

See Table 1 for remainder of key.

Table 5—

Results of antimicrobial susceptibility testing of Enterococcus spp and Staphylococcus spp isolated from the same VTH surfaces and areas in Table 1.

SpeciesNo. (%) of isolates
TotalResistant to ≥ 1 antimicrobialPentaresistant
Enterococcus spp75 (100)71 (94.7)14 (19.7)
Enterococcus faecium45 (60.0)43 (95.6)13 (30.2)
Enterococcus faecalis27 (36.0)26 (96.3)1 (3.8)
Enterococcus durans3 (4.0)2 (66.7)0 (—)
Staphylococcus spp110 (100)70 (63.6)17 (24.3)
S aureus8 (7.3)2 (25.0)1 (50.0)
SIG36 (32.7)19 (52.8)1 (5.3)
CoNS66 (60.0)49 (74.2)15 (30.6)

Isolates classified as SIG included Staphylococcus pseudintermedius, Staphylococcus intermedius, Staphylococcus delphini, Staphylococcus schleiferi subsp coagulans, Staphylococcus hyicus, and Staphylococcus lutrae. Isolates classified as CoNS included Staphylococcus epidermidis, Staphylococcus haemolyticus, Staphylococcus hominis, Staphylococcus warneri, Staphylococcus chromogenes, Staphylococcus xylosus, Staphylococcus saprophyticus, Staphylococcus caprae, Staphylococcus cohnii subsp ureolyticus, Staphylococcus sciuri, and Staphylococcus lugdunensis. Isolates that were resistant to ≥ 5 antimicrobials were classified as pentaresistant.

See Table 1 for remainder of key.

Among staphylococci, resistance to 3 of 3 β-lactam antimicrobials tested was detected (Table 4). Resistance of staphylococci to other classes of antimicrobials was uncommon, although resistance to 2 of 3 fluoroquinolones tested (gatifloxacin, 73/110 [66%] isolates and ciprofloxacin, 11/110 [10%] isolates) was detected. Pentaresistance was observed in 24.3% (17/70) of Staphylococcus spp isolates that were resistant to ≥ 1 antimicrobial and was largely driven by resistance among CoNS (Table 5).

The number of samples from which E faecium, E faecalis, S aureus, SIG, and CoNS were isolated and the number of pentaresistant isolates identified were summarized (Table 6). Among enterococci, pentaresistance was most commonly detected in E faecium (13/45 [28.9%] samples). A pentaresistant isolate was recovered from every surface in which E faecium was isolated, with the exception of samples collected from door handles and keyboards. Pentaresistant E faecium were detected in samples from multiple surfaces. The highest prevalence of pentaresistant CoNS was detected in samples from telephones (9/25) and cages (2/13). Very few samples contained pentaresistant isolates of E faecalis, S aureus, or SIG.

Table 6—

Distribution of samples from which E faecium (n = 45), E faecalis (27), S aureus (8), SIG (36), and CoNS (66) were isolated from selected surfaces and areas of a VTH and number of samples in which these isolates were found to be pentaresistant.

VariableE faeciumE faecalisS aureusSIGCoNS
TotalNo. in which isolate was pentaresistantTotalNo. in which isolate was pentaresistanTotalNo. in which isolate was pentaresistanceTotalNo. in which isolate was pentaresistantTotalNo. in which isolate was pentaresistant
Surface
 Cages1731304170132
 Treatment floor5310105030
 Door handles301001010
 Examination tables00103021
 Floor drains42300021
 Keyboards5001010112
 Telephones2140100259
 Scale6241015150
 Other321004040
Area
 Soft tissue and internal medicine ward12215120231161
 ECC ward12520316061
 Orthopedic ward206602040122
 Surgery preparation and recovery rooms030020103
 Surgery operating room and office10101010228

See Tables 1, 2, and 5 for remainder of key.

Susceptibility to tetracycline and ampicillin was detailed for E faecium and E faecalis isolated from selected surfaces throughout the VTH (Table 7). Overall, the MIC90 for E faecium was the highest concentration tested for both antimicrobials (≥ 16 μg/mL), and the MIC50 of these organisms isolated from the cages, treatment floor, and floor drains was also the highest concentration tested. Isolates of E faecalis, in general, appeared to be less resistant to tetracycline than were E faecium isolates, and resistance to ampicillin was not detected at all for E faecalis.

Table 7—

Minimum inhibitory concentrations of tetracycline and ampicillin for E faecalis and E faecium isolated from selected surfaces at a VTH.

OrganismSurfaceNo. of isolatesMIC (μg/mL)
TetracyclineAmpicillin
RangeMIC50MIC90RangeMIC50MIC90
E faeciumScale62 to ≥ 169≥ 160.25 to > 168.5> 16
 Cages17≤ 2 to ≥ 16≥ 16≥ 160.5 to > 16> 16> 16
 Treatment floor5< 2 to ≥ 16≥ 16≥ 160.5 to > 16> 16> 16
 Keyboards52 to > 162> 161 to > 161> 16
 Floor drains48 to > 16> 16> 161 to > 16> 16> 16
 Telephones2≤ 2 to > 169> 162 to > 169> 16
E faecalisScale42 to > 162> 161*11
 Cages132 to ≥ 162≥ 160.5 to 111
 Treatment floor1> 16*> 16> 161*11
 Keyboard0
 Floor drains32*221*11
 Telephones42 to > 162> 161*11

All values were the same (there was no range).

Gatifloxacin, erythromycin, and oxacillin susceptibility of SIG and CoNS isolated from selected surfaces were summarized (Table 8). Resistance among SIG isolates was not frequently detected, regardless of the sample collection surface and antimicrobial tested, however intermediate resistance was observed. The MIC90 of oxacillin for SIG isolated from the scale (8 μg/mL) was in the range indicative of resistance; however, the MIC50 of this antimicrobial for the same isolates from this surface (2 μg/mL) was still in the range indicative of susceptibility. Additionally, all SIG isolates had intermediate resistance to gatifloxacin (MIC50 and MIC90, ≤ 1 μg/mL), regardless of the sample collection surface. Resistance observed among CoNS had no apparent pattern; however, surfaces with the largest number of isolates (cages, keyboards, and telephones) were the sources of CoNS with the highest apparent resistance to oxacillin. Additionally, isolates of CoNS from most surfaces were intermediately resistant to erythromycin (MIC50, MIC90, or both > 4 μg/mL). Isolates of CoNS obtained from the scale were more variable because 2 of 5 had intermediate resistance to gatifloxacin (< 1 μg/mL). Although 1 MRSA isolate was recovered (from a cage), only 2 of 8 S aureus isolates were resistant to ≥ 1 antimicrobial tested and only 1 isolate had pentaresistance.

Table 8—

Minimum inhibitory concentrations of gatifloxacin, erythromycin, and oxacillin for SIG and CoNS isolated from selected surfaces at a VTH.

OrganismSurfaceNo. of isolatesMIC (μg/mL)
GatifloxacinErythromycinOxacillin
RangeMIC50MIC90RangeMIC50MIC90RangeMIC50MIC90
SIGScale15≤1*≤1≤1≤ 0.25 to 4< 0.250.25≤ 0.25 to 828
 Cages7≤1*≤1≤1≤ 0.25≤ 0.25≤ 0.25≤ 0.25*≤ 0.25≤ 0.25
 Treatment floor5≤1*≤1≤1≤ 0.25 to 4< 0.254≤ 0.25 to 0.5≤ 0.250.5
 Examination tables3≤1*≤1≤1≤ 0.25 to 4< 0.254≤ 0.25*≤ 0.25≤ 0.25
 Keyboards1< 1*< 1< 1< 0.25< 0.25< 0.25< 0.25*< 0.25< 0.25
CoNSScale5≤1*< 1< 1< 0.25 to 0.50.50.5≤ 0.25*≤ 0.25≤ 0.25
 Cages13≤ 1 to 424≤ 0.25 to ≥ 40.5> 4≤ 0.25 to ≥ 8≤ 0.25≥8
 Treatment floor3≤1*≤1≤10.25 to > 4> 4> 4< 0.25 to 20.52
 Examination tables2< 1 to 81.58< 0.25 to > 42.125> 4< 0.25 to 21.1252
 Keyboards11≤ 1 to 2≤ 12≤ 0.25 to > 4> 4> 4< 0.25 to > 84> 8
 Floor drains2< 1*< 1< 1> 4> 4> 41*11
 Telephones25≤ 1 to > 814< 0.25 to > 4> 4> 4< 0.25 to ≥ 81> 8

See Tables 5 and 7 for remainder of key.

Changes in prevalence of antimicrobial-resistant isolates over time—Results of susceptibility testing for isolates recovered from the scale at various time points were summarized (Table 9). Not all species were isolated at all sample collection times, and only data for E faecium, E faecalis, and SIG isolates were summarized. Between the first and second sample collection times (ie, times at which E faecium was isolated), resistance of E faecium was apparently increased for all antimicrobials tested except vancomycin and gatifloxacin (to which isolates remained susceptible) and levofloxacin, daptomycin, linezolid, and rifampin (for which resistance decreased or remained unchanged). In contrast, antimicrobial susceptibility of E faecalis was mostly unchanged; however, isolates were susceptible to tetracycline (MIC50, 2 μg/mL) and erythromycin (MIC50, 0.25 μg/mL) at the first time point and were resistant to tetracycline (MIC50, > 16 μg/mL) and intermediately resistant to erythromycin (MIC50, 1 μg/mL) at the second time point. Isolates of E faecalis remained resistant to quinupristin-dalfopristin over time (MIC50, ≥ 4 μg/mL), but were resistant to rifampin at the first time point (MIC50, 4 μg/mL) and intermediately resistant at the second time point (MIC50, 2 μg/mL). At 7 of the 13 sample collection times, SIG organisms were isolated from the scale. Although the numbers were too small for statistical evaluation, the overall degree of antimicrobial resistance appeared to remain stable, with a few sporadic peaks.

Table 9—

The MIC50 (μg/mL) of various antimicrobials for E faecium, E faecalis, and SIG isolated from 1 scale at a VTH at various time points between February 5, 2007, and December 29, 2009.

Class and antimicrobialE faeciumE faecalisSIG
10/0704/0810/0710/0907/0710/0701/0804/0801/0903/0909/09
Aminoglycoside
 GentamicinNINININI222216< 2< 2
Cephalosporin
 CeftriaxoneNINININI8888< 8< 8< 8
Fluoroquinolone
 Ciprofloxacin12110.50.50.50.5< 0.5< 0.51
 Gatifloxacin121< 11111< 1< 1< 1
 Levofloxacin22210.250.250.250.25< 0.25< 0.250.5
Glycopeptide
 Vancomycin12121111< 1< 1< 1
Lincosamide
 ClindamycinNINININI< 0.120.12< 0.12< 0.12< 0.12< 0.12< 0.12
Lipopeptide
 Daptomycin4211< 0.25< 0.25< 0.25< 0.25< 0.25< 0.25< 0.25
Macrolide
 Erythromycin1> 40.2510.251.50.250.25< 0.25< 0.25< 0.25
Oxazolidinone
 Linezolid211.511111111
β-Lactam
 Ampicillin0.25> 16110.1240.120.120.12< 0.12< 0.12
 OxacillinNINININI0.2540.250.25< 0.25< 0.25< 0.25
 Penicillin0.5> 8440.1240.120.120.250.120.12
Rifampin
 Rifampin40.5420.50.50.50.5< 0.5< 0.5< 0.5
Streptogramin
 Quinupristin-dalfopristin144> 40.120.120.120.12< 0.12< 0.12< 0.12
Sulfonamide
 Trimethoprim-sulfamethoxazoleNINININI0.50.50.50.5< 0.5< 0.5< 0.5
Tetracycline
 Tetracycline2> 162> 16222162> 162

The collection times shown indicate all instances in which these organisms were isolated from the scale. When > 1 isolate was obtained from the scale at the same sample collection time, a single isolate was selected for testing.

See Tables 4 and 5 for remainder of key.

PFGE analysis—The PFGE patterns for isolates of E faecium represented 6 clones, and the patterns for E faecalis isolates represented 1 clone (Figure 1). Enterococcus faecium clone A comprised 2 isolates from 2 types of surfaces (scale and treatment floor) and areas of the VTH. Clone B consisted of 2 isolates from 1 type of sample surface (cages), but these isolates differed in their antimicrobial susceptibility patterns. Clones C, D, and E consisted of 1 isolate of E faecium each. Enterococcus faecalis clone F consisted of 2 isolates from the same type of sample surface (scale), but these also differed in their antimicrobial susceptibility patterns.

Figure 1—
Figure 1—

Composite image of PFGE patterns for 7 isolates of Enterococcus faecium (lanes 1 to 7) and 2 isolates of Enterococcus faecalis (lanes 8 and 9) collected from surfaces in a VTH. Enterococcus faecium clone A comprised 2 isolates (1 from the scale in the soft tissue and internal medicine ward and 1 from the treatment floor in the ECC ward). Clone B consisted of 2 isolates from the same type of surface (cages), but these had different antimicrobial susceptibility patterns. Clones C, D, and E each consisted of 1 isolate of E faecium. Enterococcus faecalis clone F comprised 2 isolates from the same surface (scale) that had different antimicrobial susceptibility patterns. M = DNA marker pattern.

Citation: Journal of the American Veterinary Medical Association 240, 12; 10.2460/javma.240.12.1463

Discussion

Bacteria are present in any hospital environment; however, the presence of pathogenic or antimicrobial-resistant bacteria can allow the transmission cycle of such bacteria to persist. Various species of pathogenic and nonpathogenic enterococci and staphylococci were isolated from selected surfaces and areas throughout the VTH of the present study, and antimicrobial resistance was apparently increased in some of the isolates collected from 1 surface (a weight scale) during the course of the study. Additionally, clinically important bacteria were identified, including MRSA.

Among surfaces, the scale had the highest prevalence of enterococci and staphylococci and also had the highest likelihood of bacterial isolation in univariate and multivariate analysis. In the VTH of the present study, the scale was located in the soft tissue and internal medicine ward, which was the area with the highest prevalence of bacterial isolation and was significantly associated with isolation of Enterococcus spp and Staphylococcus spp during univariate analysis. Although cages did not have the highest prevalence of either type of bacteria, this category of surface remained significantly associated with isolation of enterococci or staphylococci in multivariate logistic regression analysis. Cages selected for sample collection in the present study were located in many areas, including the soft tissue and internal medicine, ECC, and orthopedic wards and surgery recovery rooms. Univariate analysis revealed a significant likelihood of isolating enterococci from the soft tissue and internal medicine and ECC wards and staphylococci from the soft tissue and internal medicine ward; however, these associations were not significant when surface was included in the model. These results suggest that cage surfaces specifically, rather than the location of those cages within the VTH, had the largest impact on isolation of these organisms and should be a focus for targeted infection control.

It is interesting to note that areas within the VTH did not remain significantly associated with isolation of staphylococci or enterococci when surface and area were analyzed in the same model, whereas many surfaces throughout the VTH continued to be significantly associated with this variable. This also suggests that these associations were driven more by the sample collection surface than by a particular area within the VTH. This type of observation is important when considering infection control protocols and suggests that the practice of uniform procedures for surface-specific cleaning and disinfecting should be encouraged, regardless of the hospital area in which the surface is located.

Staphylococci were isolated from 15.8% (68/430) of the samples collected in the present study, and the likelihood of isolation of these organisms was significant for most sample collection surfaces. The species most commonly identified were CoNS (66/110 [60%] isolates); antimicrobial resistance (49/66 [74.2%]) and pentaresistance (15/49 [30.6%]) of antimicrobial-resistant isolates appeared to be more prevalent among CoNS than among S aureus (2/8 isolates with antimicrobial resistance and 1/2 with pentaresistance) and SIG (19/36 [52.8%] isolates with antimicrobial resistance and 1 with pentaresistance). Previous studies8,14 in which staphylococci on environmental surfaces of a VTH were evaluated found increased prevalence on surfaces that health-care workers' hands were most likely to come in contact with. Although results of the present study revealed an increased likelihood of isolation of staphylococci from these types of surfaces (eg, examination tables and keyboards), the greatest likelihood of detecting staphylococci was determined for the treatment floor (OR, 26.70; 95% CI, 3.54 to 201.61) and scale (OR, 30.798; 95% CI, 4.04 to 235.698) in the multivariate analysis. Health-care providers' hands would be less likely to come into direct contact with the treatment floor and scale surface than with many others because the treatment floor is an area in which larger animals are kept during treatment in the ECC and the scale is used to weigh animals. However, there is ample opportunity for fecal (eg, animal sitting or lying) and oral (eg, animal lying with head down) contamination of these surfaces by animals. This finding exemplifies some of the inherent differences between surfaces in human and veterinary hospitals. Infection control practices in veterinary hospitals must be tailored to the unique nature of the veterinary hospital environment.

Although only 8 S aureus isolates were identified, 1 MRSA isolate was cultured from a sample from a cage. It was not determined whether the dog housed in that cage at the time of sample collection was colonized with MRSA. Results of a previous study4 indicated the presence of MRSA in patient housing units at a VTH, independent of the inhabitant's MSRA status. Although those results were reported for large-animal housing facilities after an outbreak of MRSA, it is important to note that MRSA was isolated from 6.9% of stalls housing horses that tested negative for MRSA.4 In another study,10 investigators found MRSA belonging to, or closely related to, 1 epidemic strain in dogs and staff and on environmental surfaces at a VTH. These findings reveal the ease with which pathogens can be transferred in a VTH and the importance of the role that environmental surfaces can have in this process.

The antimicrobial resistance detected in E faecium isolates of the present study should be of concern because E faecium is an important pathogen in both human and animal medicine. Although the likelihood of isolating enterococci from many surfaces throughout the VTH was apparently much lower than that for staphylococci, pentaresistance was detected in 28.9% (13/45) of the E faecium isolates. Additionally, the MIC90 and most of the MIC50 values of tetracycline and ampicillin for E faecium were the highest concentrations tested. Results of PFGE analysis included the identification of 1 clone of E faecium isolated from samples collected from 2 surfaces (the scale and the treatment floor) on the same day. Most animals entering the VTH of the present study were weighed on the scale before being taken to a specific examination or treatment area. It is likely that an animal was weighed on the scale and then placed on a mat on the treatment floor (a typical pattern for many larger, more critically ill patients). The scale surface in the present study was made of a rubber material and underwent infrequent cleaning at the time these samples were collected.

Although no isolates of enterococci in the present study were resistant to vancomycin, 3 had intermediate resistance and 2 isolates of E faecalis with intermediate resistance to vancomycin were isolated from cages and the treatment floor. Investigators in a previous study15 reported that isolates of vancomycin-resistant enterococci were transferred to 10.6% of previously disinfected surfaces after being touched by a nurse during routine tasks in a human hospital. Frequent contact between health-care providers' hands and the treatment floor in the present study was unlikely; however, cage surfaces were likely to have a high degree of physical contact with animals and to be touched by health-care providers. Animals at the VTH were primarily housed in cages, and health-care providers opening the cage without gloves would have the opportunity to deposit or pick up contaminants and transmit bacteria.

Although many studies have reported isolation of pathogenic bacteria from either human or veterinary hospitals, the role of environmental surfaces in continuing the cycle of health-care–associated transmission of such pathogens is unknown. The authors of a previous study14 stated that although the role of environmental surfaces as vectors in the transmission of pathogens in both human and veterinary clinics is gaining more attention, it is not the major contributing factor and that health-care worker hygiene should be the focus of efforts to control the spread of infection. Considering sample collection surfaces in the present study that health-care providers would be expected to be in contact with most frequently, we identified an increased likelihood of isolating enterococci (5/26 [19.2%] samples; OR, 6.90; 95% CI, 1.23 to 38.70) and staphylococci (9/26 [34.6%]; OR, 7.07; 95% CI, 1.28 to 39.13) from computer keyboards, compared with all other surfaces evaluated. In other studies,9,16 various health-care–associated pathogens were isolated from 24% to 31% of keyboards sampled. Investigators in one of those studies9 specifically evaluated bacteria present on computer keyboards within a VTH and compared results with the cleaning schedules reported for the facilities where samples were collected. Staphylococcus aureus was not isolated in that study,9 although 92.7% of samples tested positive for the presence of bacteria, mostly commensal organisms found on dog and cat skin. Cleaning practices were reportedly inconsistent, and the authors noted that although disinfectants were used to clean cages and tables, keyboards were often neglected completely or were cleaned with household cleaners. Many computer users, regardless of profession, may eat or drink as they type. Additionally, commonly used objects such as keyboards may be accessed by health-care providers during patient care but are not a direct instrument used for routine patient care and therefore may not be considered a focus of infection control or a cause for handwashing before or after use.

It is important to consider potential limitations of the study reported here. Swabs were used to collect environmental surface samples, and this may limit comparability with results of other studies in which investigators used gauze or agar strips or slides. There are several absorptive media available for sample collection purposes, but either wipes or swabs are preferred.17 Additionally, although samples were collected from the same surfaces at different time points and the same methods were used to collect samples throughout the study, steps were not taken to ensure the same amount of surface area was swabbed. We did not concurrently monitor practices that could potentially affect the presence of organisms on tested surfaces, such as cleaning schedules or the use of antimicrobials in the facility prior to or during the study. Finally, the presence of epidemiologically linked isolates was investigated via PFGE, but this was not done for all isolates from all surfaces. We believe that the limited data from this analysis highlight the evidence of transmission of resistant organisms within a VTH and give support for further, more in-depth analyses.

The study reported here included collection of samples during a 3-year period and involved extensive procedures to identify all species of enterococci and staphylococci isolated, whereas a similar previous study8 reported enterococci and staphylococci only at the genus level. Additionally, susceptibility testing in the present study included antimicrobials used in both human and veterinary medicine. This allowed for identification of antimicrobial resistance that could presumably originate in microbes transmitted by either host.

Definitive standards for infection control in VTHs are lacking. A study18 of VTHs at AVMA Council on Education–accredited colleges of veterinary medicine showed that although infection control is a stated priority, formalized training and education are lacking and staff members are likely to gravitate toward procedures for their convenience and not necessarily for their effect on infection control. Additionally, an internal studyk of health-care provider perception and the use of infection control practices within the Michigan State University VTH indicated that most health-care providers acknowledge that infection control protocols would be beneficial for faculty, staff, students, patients, and clients; however, less than half of all small animal faculty and staff had read the infection control protocols. There were also conflicting opinions about whether resources and administrative support were sufficient to allow the implementation of infection control protocols. During the early months of the present study, a preliminary set of the data reported here was presented to staff at the VTH, illustrating that the scale had the highest detected prevalence of enterococci and staphylococci. Anecdotal reports indicated that a cleaning regime for the scale was initiated as a result of that presentation, followed by complete removal of the surface material (which was replaced with stainless steel after the study was completed). Although we were unable to document and assess these changes, the information suggests that data such as these can be used to enhance infection control policies.

In addition to evaluation of the prevalence of bacteria and changes in antimicrobial susceptibility over time, future studies in VTH environments should include assessment of daily infection control practices. Identification of the scale as a surface with high prevalence and high likelihood of isolation of staphylococci and enterococci suggests that commonly used surfaces such as this may be an important primary focal point for infection control studies.

ABBREVIATIONS

ATCC

American Type Culture Collection

CI

Confidence interval

CoNS

Coagulase-negative staphylococci

ECC

Emergency and critical care

MIC50

Minimum inhibitory concentration for 50% of isolates tested

MIC90

Minimum inhibitory concentration for 90% of isolates tested

MRSA

Methicillin-resistant Staphylococcus aureus

PFGE

Pulsed-field gel electrophoresis

SIG

Staphylococcus intermedius spp group

VTH

Veterinary teaching hospital

a.

Becton, Dickinson and Co, Franklin Lakes, NJ.

b.

API 20 Strep identification strips, bioMérieux Inc, Durham, NC.

c.

API 20 Strep Analytical Profile Index, bioMérieux Inc, Durham, NC.

d.

API 20 Staph identification strips, bioMérieux Inc, Durham, NC.

e.

API 20 Staph Analytical Profile Index, bioMérieux Inc, Durham, NC.

f.

Sensitire microdilution system, TREK Diagnostic Systems Inc, Cleveland, Ohio.

g.

GPN3F gram-positive MIC plate with tigecycline, TREK Diagnostic Systems Inc, Cleveland, Ohio.

h.

AutoReader, TREK Diagnostic Systems Inc, Cleveland, Ohio.

i.

CHEF-DR III, Bio-Rad Laboratories, Hercules, Calif.

j.

SAS, version 9.1.3, SAS Institute Inc, Cary, NC.

k.

Miller K, Bolin C, Stobierski MG, et al. Infection control knowledge, attitudes and practices of VTH faculty and staff, and CVM students (abstr), in Proceedings. Annu Phi Zeta Res Day 2010; 9–10.

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