Methicillin-Resistant Staphylococcus aureus spa Type t002 Outbreak in Horses and Staff at a Veterinary Teaching Hospital after Its Presumed Introduction by a Veterinarian

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) infection and colonization, involving MRSA strains which differ from common human health care-associated clones, have become serious emerging conditions in equine veterinary hospitals. In 2010, MRSA spa type t535 caused an outbreak involving both horses and personnel in a veterinary teaching hospital in Israel. Since then, surveillance continued, and occasional MRSA isolation occurred. Two years later, MRSA of another spa type, t002, was isolated from a veterinarian and, 3 weeks later, from a horse. The appearance of spa type t002, a common clone in human medicine in Israel, among both personnel and horses, prompted a point-prevalence survey of hospital personnel and hospitalized horses. Fifty-nine staff members (n = 16 equine; n = 43, other) and 14 horses were screened. Ten of 59 staff members (16.9%) and 7 of 14 horses (50%) were MRSA carriers. Among the staff, 44% of large animal department (LAD) personnel, compared with only 7% of non-LAD personnel, were carriers. Isolates from all horses and from 9 of 10 personnel were found to be of MRSA spa type t002. This clone was later isolated from an infected postoperative wound in a hospitalized horse. Measures were taken to contain transmission between horses and personnel, as was done in the previous outbreak, resulting in reduction of transmission and, finally, cessation of cross-transmission between horses and personnel.

INTRODUCTION

Methicillin-resistant Staphylococcus aureus (MRSA) infection or colonization has become a serious emerging condition in equine veterinary hospitals. In recent years, outbreaks involving both horses and humans have been reported in veterinary hospitals in the United States (1), Canada (2), Ireland (3), Austria (4, 5), the Netherlands (6), Switzerland (7), and, recently, Israel (8). MRSA strains recovered from companion animals are generally similar to human nosocomial MRSA, whereas strains recovered from food animals appear to belong to specific animal-adapted clones, unrelated to most common health care-associated MRSA (9). In recent years, livestock-associated MRSA (LA-MRSA) was significantly associated with veterinarians in contact with livestock (10). Among veterinarians, LA-MRSA carriage rates were 7.5% in Belgium and 1.4% in Denmark (10). Similarly to strains in food animals, most MRSA isolates from horses and associated personnel differ from common health care-associated MRSA strains (11). This finding was demonstrated in an outbreak at the Koret School of Veterinary Medicine-Veterinary Teaching Hospital (KSVM-VTH) in Israel, where a rare MRSA strain, spa type t535, was found to cause wound infections in hospitalized horses and to have spread extensively among other hospitalized horses as well as among personnel caring for them (8). As recommended (12), strict infection control measures were implemented, horses infected or colonized with MRSA were isolated, and decolonization of personnel was carried out. These steps succeeded; indeed, 6 months after the intervention, personnel and hospitalized horses were all MRSA negative (8). Following that outbreak, passive surveillance was continued. In each case of wound infection, a swab was sent for culture. Occasional MRSA isolation prompted personnel screening, typing, and implementation of control measures to contain transmission among horses and staff. In the context of such screening, MRSA spa type t002 was isolated from a clinician in the hospital's large animal department (LAD) in April 2012. This clinician remained a carrier for 7 months (over 5 different sampling dates). Two weeks later, MRSA spa type t002 was isolated from another LAD clinician, and it was isolated a week later, for the first time, from a horse. Screening continued, and an additional LAD staff member in the following month was found to be a carrier of MRSA spa type t002. In the screening of hospitalized horses following the discovery of MRSA spa type t002, over a period of 4 months, 21 additional horses were found to be carriers, and spa typing in 14 of these horses revealed type t002 (for the other horses, the spa type was not determined). The appearance of MRSA of a spa type other than t535, i.e., t002, among both horses and personnel prompted a decision to screen staff and hospitalized horses to determine the extent of cross-transmission with this strain between staff and hospitalized horses.

MATERIALS AND METHODS

Outbreak investigation: horses and personnel.

The initial survey was conducted in September 2012, nearly 2 years after the conclusion of the intervention that ended the previous MRSA outbreak. MRSA surveillance was conducted among personnel from the LAD and from other departments in the KSVM-VTH and also from hospitalized horses. Fifty-nine KSVM-VTH staff members (n = 16, LAD; n = 43, other) and 14 horses (all hospitalized horses) were screened. Samples from both staff and horses were taken from both nares by inserting a cotton-tipped swab and retracting while rotating the swab in contact with the nasal mucosa (6). Carriage and noncarriage were defined by the presence or absence, respectively, of MRSA as determined by work-up of the nasal swab, as described below. The study was approved by the jurisdictional ethical review board and by the ethics committee of the Koret School of Veterinary Medicine, Hebrew University, and sample collection was performed with individual consent.

Microbiological and molecular methods.

Nasal swabs obtained from each human and horse subject were plated on ChroMagar MRSA plates (ChroMagar, Paris, France). Dark pink colonies suspected of being MRSA were subcultured onto blood agar plates (Hy Labs, Rehovot, Israel) and further tested for coagulase production using the Prolex Staph Xtra latex kit (Pro-Lab Diagnostics, Richmond Hill, Ontario, Canada) and for DNase production using DNase agar plates (Novamed, Jerusalem, Israel). Isolates suspected of being MRSA after the initial testing were submitted for definitive identification and antimicrobial susceptibility testing (AST) by Vitek 2 (bioMérieux, Marcy l'Etoile, France). Antimicrobial susceptibility breakpoints were determined according to the Clinical and Laboratory Standards Institute guideline (13). Genetic relatedness of strains was determined by spa typing (14). Spa types were determined with Ridom StaphType software version 2.2.1 (Ridom GmbH, Würzburg, Germany). In addition, pulsed-field gel electrophoresis (PFGE) was performed for t002 isolates (15). Representative pulsotypes were subjected to PCR for the Panton-Valentine leukocidin (pvl) gene (16) and to staphylococcal cassette chromosome mec element (SCCmec) typing, with type assigned according to the mec and ccr complexes (17).

Decolonization protocol.

All LAD personnel and other non-LAD personnel found to be MRSA carriers were prescribed 1 week of daily 4% chlorhexidine soap (Septal Scrub, Teva, Ashdod, Israel) showers and thrice daily administration of 2% intranasal mupirocin (Bactroban Nasal Ointment; GlaxoSmithKline, Ltd., Petach Tikva, Israel).

Follow-up screening: horses and personnel.

During the ensuing months, repeated samples were collected from personnel and hospitalized horses in order to determine posttreatment carriage status.

RESULTS

Ten of 59 staff members (16.9%) were found to be MRSA carriers. Of these, 7 were working in the LAD (carriage rate among LAD staff members screened, 7 of 16, or 44%) and 3 were working in other departments (carriage rate among non-LAD staff members screened, 3 of 43, or 7%). One of these 3 non-LAD staff members was an anesthesiologist who treats horses during surgery. Seven of 14 horses (50%) were also MRSA carriers.

MRSA types.

Isolates from all horses and from 9 of 10 personnel were found to be MRSA spa type t002. All of these isolates had an identical PFGE pattern, with the exception of 2 isolates identified in 2 non-LAD personnel, a veterinary student and a technician from another section of the hospital (Figure 1). The MRSA spa type t002 isolates were characterized as SCCmec type II and were negative by pvl-PCR. AST results indicated resistance to erythromycin, clindamycin, ciprofloxacin, and gentamicin (dominant strain only) and susceptibility to mupirocin, trimethoprim-sulfamethoxazole, linezolid, rifampin, and vancomycin. One LAD clinician was a carrier of MRSA spa type t127; prior screening had shown him to be a long-term carrier of MRSA of this spa type.

FIG 1.

Pulsed-field gel electrophoresis (PFGE) of MRSA isolates of spa type t002 isolated from staff and horses at the Koret School of Veterinary Medicine-Veterinary Teaching Hospital. All isolates had an identical PFGE pattern (clone A), with the exception of 2 isolates identified in 2 non-LAD personnel (clone A*), which had a 3-band difference from the dominant clone.

Intervention and follow-up screening.

Decolonization treatment was initiated for all LAD personnel and for the 3 other staff members found to be MRSA carriers. MRSA-colonized horses were placed in contact isolation, in which entrance to the stall was allowed only in protective gear (coveralls, gloves, shoe covers), and infection control protocols were reinforced. Follow-up screening of LAD personnel and hospitalized horses was carried out at approximately 2-month intervals, with discharge or isolation of carrier horses and decolonization recommended to carrier personnel. At each sampling date, all available LAD personnel were screened, as were all hospitalized horses.

In November 2012 (2 months after the initial survey), 4 of 24 LAD personnel screened (16.7%) were MRSA carriers, as were 1 of 11 horses (9.1%). Three of the isolates from personnel and the equine isolate were spa type t002. In December, MRSA spa type t002 was isolated from an infected postoperative wound in 1 horse. In January 2013 (4 months after the initial survey), 2 of 33 personnel (6.1%) were MRSA carriers (spa type t002). In March 2013 (6 months after the initial survey), 1 of 18 personnel (5.6%) and 1 of 21 hospitalized horses (4.8%) were MRSA carriers; in both cases, MRSA was spa type t002. In May 2013 (8 months after the initial survey), 1 of 16 personnel (6.3%) was a MRSA carrier, and again in June 2013 (9 months after the initial survey), 1 of 16 personnel (the same person) was a carrier. This staff member, a technician, had been a carrier in the past, underwent successful decolonization, and again underwent successful decolonization after this result. At the time of the June 2013 survey, none of the 19 hospitalized horses was a carrier.

DISCUSSION

In recent years, MRSA has become one of the most important nosocomial pathogens affecting equine veterinary hospitals (18). The cross-transmission of MRSA between hospitalized horses and veterinary staff in the 2010 outbreak at our hospital (8) resulted in increased awareness of this pathogen among hospital personnel. Infection control measures were implemented and strict protocols were enforced in order to decrease the risk for recurrence. Since that outbreak, passive surveillance, in which we test horses in which MRSA infection is suspected, was continued, and, in each case of postoperative wound infection in a horse, a swab was sent for culture and antimicrobial susceptibility testing. Reappearance of MRSA in samples collected from horses and personnel in the veterinary teaching hospital was not unexpected, as it has been demonstrated that MRSA is constantly introduced and frequently found in an equine veterinary hospital environment (18). Among the MRSA strains that have been described are ST8 (Canadian MRSA-5/USA-500 epidemic MRSA strain) and ST254, which are suggested to be horse adapted (19). In contrast, MRSA spa type t535, which caused the 2010 outbreak, is not known to colonize horses and is also exceedingly rare in humans (8).

Three scenarios for MRSA environmental contamination in veterinary hospitals were recently suggested: constant introduction and reintroduction of strains, circulation of clones throughout the hospital services, and maintenance of strains over time in the environment (18). The appearance of MRSA spa type t002, in April 2012, is an example of the introduction of a new strain not previously isolated from a horse in the KSVM-VTH, which soon circulated in the LAD, colonizing both horses and staff and even manifesting clinically, as evidenced by isolation from a contaminated postoperative wound in a hospitalized horse. MRSA spa type t002 is the third most common type, accounting for 6.79% of all isolates submitted to the Ridom database (20). MRSA spa type t002 is common in human medicine in Israel, as illustrated in a survey of MRSA clinical isolates from 5 hospitals across Israel, in which type t002 was the second most common type, accounting for 26% of all isolates (21). To our knowledge, this is the first time that MRSA spa type t002 has been isolated from horses. Given the epidemiology of type t002 in human medicine and its appearance at our hospital among LAD personnel prior to its appearance among horses, we believe that the current outbreak was precipitated by the introduction into the hospital environment of MRSA spa type t002 by a colonized staff member. It is possible that MRSA spa type t002 is less adapted and pathogenic to horses than are other strains of MRSA, since it manifested clinically only once during all the months that it was present in the LAD among both horses and personnel.

Measures were taken to contain transmission between horses and personnel, including decolonization treatment of carrier personnel, enforcement of infection control measures, isolation of all horses colonized or infected with MRSA, discharge of these horses as soon as medically feasible, and intensive environmental cleaning and disinfection (12). These steps, as in 2010, again resulted in reduction of transmission and, finally, cessation of cross-transmission of MRSA between horses and personnel. Furthermore, the flooring of both the recovery room and the treatment room was removed and thoroughly cleaned, following which new rubber mats were installed. In order to detect such outbreaks early, all horses ideally would be screened at admission and discharge; however, this approach is impractical and expensive (6). We did make a decision not to rely exclusively on testing of involved horses with suspected MRSA infection (passive surveillance), but also to screen all hospitalized horses for MRSA carriage every 3 months (active surveillance) and thereby potentially detect a future outbreak at an early stage.

In a recent study, it was suggested that the nasal vestibulum, rather than the ventral meatus, which we sampled, is the optimal sampling site (22). It is therefore possible that the true MRSA carriage prevalence among hospitalized horses was actually higher than the percentage we reported.

The MRSA clones that caused the two outbreaks in the KSVM-VTH differ from those reported to be responsible for similar outbreaks in North America and in Europe. Currently, it appears that horses are not an important source of community-associated MRSA in Israel, as was also seen in a survey in which 206 farm horses were sampled and all were MRSA negative (S. Tirosh-Levy, personal communication). These findings differ from those found among horses presenting to a Belgian equine clinic, where 12 of 110 horses screened (10.9%) were found to be MRSA carriers (23). Moreover, ongoing surveillance of MRSA isolated from clinical and screening cultures in the veterinary teaching hospital has not identified strains commonly found in horses. These epidemiological differences may result from differences in management between the Israeli equine industry and its counterparts in Europe and North America or from other environmental or demographic variables.