Elsevier

Veterinary Microbiology

Volume 167, Issues 3–4, 27 December 2013, Pages 680-685
Veterinary Microbiology

Short communication
Identification and characterization of methicillin-resistant Staphylococcus aureus, Staphylococcus epidermidis, Staphylococcus haemolyticus and Staphylococcus pettenkoferi from a small animal clinic

https://doi.org/10.1016/j.vetmic.2013.07.036Get rights and content

Abstract

The aim of this study was to isolate and characterize methicillin-resistant staphylococci (MRS) in a small animal clinic and to investigate their distribution and possible transmission. Swabs (n = 72) were taken from hospitalized pets, the environment and employees of a small animal clinic and screened for the presence of MRS. The staphylococcal species was confirmed biochemically or by 16S rDNA sequencing. Susceptibility to antimicrobial agents was tested by broth dilution. The presence of mecA and other resistance genes was confirmed by PCR. Molecular typing of the isolates followed standard procedures. In total, 34 MRS belonging to the four species Staphylococcus aureus (n = 5), Staphylococcus epidermidis (n = 21), Staphylococcus haemolyticus (n = 6) or Staphylococcus pettenkoferi (n = 2) were isolated. All isolates were multidrug-resistant with resistance to at least three classes of antimicrobial agents. Among the five methicillin-resistant S. aureus (MRSA) isolates, four belonged to the clonal complex CC398; two of them were isolated from cats, the remaining two from pet cages. Overall, the MRS isolates differed in their characteristics, except for one S. epidermidis clone (n = 9) isolated from hospitalized cats without clinical staphylococcal infections, pet cages, the clinic environment as well as from a healthy employee. This MRSE clone was resistant to 10 classes of antimicrobial agents, including aminocyclitols, β-lactams, fluoroquinolones, lincosamides, macrolides, phenicols, pleuromutilins, sulfonamides, tetracyclines and trimethoprim. These findings suggest a possible transmission of specific MRS isolates between animal patients, employees and the clinic environment.

Introduction

Among methicillin-resistant staphylococci (MRS), methicillin-resistant Staphylococcus aureus (MRSA) isolates – especially those of clonal complex (CC) 398 – have been found at different prevalences among different farm animal species (Feßler et al., 2012, Monecke et al., 2013). In pets, methicillin-resistant Staphylococcus pseudintermedius (MRSP) isolates have been found frequently (Weese and van Duijkeren, 2010). MRSA, but especially MRSP, often show expanded resistance to antimicrobial agents and the treatment of infections caused by these bacteria represents a real challenge for veterinary practitioners (Perreten et al., 2010, Kadlec et al., 2010). Comparatively little is known about the presence and antimicrobial resistance of methicillin-resistant members of other staphylococcal species. Animal clinics in which sick animals, that might shed pathogenic bacteria, are present and antimicrobial agents are frequently applied may constitute a suitable environment for the development and spread of multiresistant staphylococci including MRS. A screening for carriage of MRSA and MRSP of canine and feline patients before entering a small animal clinic confirmed that dogs and cats can act as vehicles and bring these bacteria into the clinic environment (Nienhoff et al., 2011a, Nienhoff et al., 2011b). The presence of MRS in animals does not only bear the risk of difficult-to-treat infections of the animals, but also constitutes a risk for the clinic employees who are in close contact with the animals and may become occupationally colonized (Guardabassi et al., 2004). Furthermore, contaminated clinic facilities can serve as a source of infections (Aksoy et al., 2010). In this regard, the stationary area within a clinic is a critical place, as animals that are vulnerable for infections are present and the selective pressure due to the use of antimicrobial agents is relatively high.

The aim of this study was to characterize MRS isolated from a small animal clinic in order to gain information about their distribution within the clinic and to investigate a possible transmission between animal patients, clinic environment and employees.

Section snippets

Isolation and identification of methicillin-resistant staphylococci

In total, 72 swabs were taken from pets (n = 10, nasopharyngeal swabs), the clinic environment (n = 58, surface swabs) and employees (n = 4, nasal swabs). Pet swabs were obtained from hospitalized animals (nine cats, one dog) exclusively, environmental swabs comprised clinic facilities in the stationary area (n = 34), the operating room (n = 15) and the consulting rooms (n = 9). After overnight enrichment in Mueller-Hinton (MH)-broth with 6.5% sodium chloride, the samples were cultured on MH-agar plates

Identification and characterization of MRS isolates

From 72 swabs taken, 34 MRS [S. aureus (n = 5), S. epidermidis (n = 21), Staphylococcus haemolyticus (n = 6), Staphylococcus pettenkoferi (n = 2)] could be isolated. These included six MRS from hospitalized cats without clinical staphylococcal infections, four MRS from healthy employees and 24 MRS from the clinic environment (Table 1). Most MRS were detected in the stationary area of the clinic whereas all samples taken from the operating room and the consulting rooms, except one from a stethoscope,

Conclusions

Although nosocomial infections due to methicillin-resistant coagulase-negative staphylococci are still only rarely reported in veterinary medicine, the adaptation of these pathogens to the clinic environment should be seen with caution. All MRS species detected in this study have already been reported as causes of wound or blood stream infections in human medicine (Mihaila et al., 2012, Yu et al., 2010) and some of them have also been described to be associated with infections in dogs and cats (

Acknowledgements

The authors thank the participating small animal clinic and Kerstin Meyer, Vivian Hensel, and Roswitha Becker for expert technical assistance. This study was financially supported by the German Federal Ministry of Education and Research (BMBF) through the German Aerospace Center (DLR), grant number 01KI1014D (MedVet-Staph).

References (32)

  • E. Aksoy et al.

    Evaluation of surface contamination with staphylococci in a veterinary hospital using a quantitative microbiological method

    J. Small Anim. Pract.

    (2010)
  • Clinical Laboratory Standards Institute

    Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals-Third Edition: Approved Standard M31-A3

    (2008)
  • M.C. Enright et al.

    Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus

    J. Clin. Microbiol.

    (2000)
  • A.T. Feßler et al.

    Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany

    Appl. Environ. Microbiol.

    (2011)
  • A. Feßler et al.

    Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis

    J. Antimicrob. Chemother.

    (2010)
  • A. Ghosh et al.

    Resident cats in small animal veterinary hospitals carry multi-drug resistant enterococci and are likely involved in cross-contamination of the hospital environment

    Front. Microbiol.

    (2012)
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