REVIEW
Methicillin—resistant Staphylococcus aureus in dogs and cats: an emerging problem?
There is concern over transmission of methicillin-resistant Staphylococcus aureus (MRSA) between animals and humans. The spread of hospital-acquired and community-acquired MRSA is a major challenge in human medicine. MRSA is rarely isolated from animals but methicillin resistance occurs in staphylococci that are more prevalent in animals. MRSA infections in animals are uncommon and most are associated with exposure to medical hospitals, extensive wounds, prolonged hospitalisation and immunosuppression. The risk to human health appears to be small but a survey of methicillin-resistant staphylococci in animals is required. Thorough investigation of possible zoonotic infections to establish linkage is encouraged. Medical and veterinary staff should appreciate that animals can carry MRSA, cooperate in eliminating infections and monitor animals in medical environments. Veterinary clinics should implement guidelines for dealing with MRSA. Responsible antibiotic use should minimise the spread of antibiotic resistance but a UK monitoring scheme is desirable.
R. A. DUQUETTE AND I. J. NUTTALL
Journal of Small Animal Practice (2004) 45, 591—597
University of Liverpool Small Animal
Teaching Hospital, Faculty of
Veterinary Science, Crown Street,
Liveroool L7 7EX
INTRODUCTION
There has been recent concern over the possible hazard to human health from carriage of strains of methicillin-resistant Staphylococcus aureus (MRSA) by companion nimals (O'Rourke 2003, Revill 2003). This article reviews the epidemiology of MRSA in humans and domestic animals (with an emphasis on dogs and cats) in order to assess the possibility of zoonotic spread and the risk to human health.
Staphylococcus aureus in humans
In humans, S aureus has long been recognised as a major pathogen causing a wide range of conditions from mild skin infections to severe bacteraemia, where complications such as endocarditis, metastatic infections and septicaemia may ensue (Lowy 1998). Despite this, S aureus is a normal commensal of the human
nasopharynx, anterior nares, perineum and skin (Kloos and Bannerman 1994). Colonisation can occur shortly after birth and recur any time thereafter, with assymptomatic carriers comprising 25 to 50 per cent of the population (Millian and others 1960, Payne and others 1965, John and others 1993). Colonisation can be transient or persistent, with some documented cases lasting for years (Sanford and others 1994).
The development of penicillin promised an effective treatment against many bacterial infections (Chain and others 1940). However, within a few years of its introduction, an enzyme produced by S aureus that inactivated the antimicrobial properties of penicillins was identified (Kirby 1944). This enzyme, now known as B-lactamase, hydrolysed the B-lactam ring structure of penicillins. Its discovery marked the beginning of staphylococcal antibiotic resistance. In the following decade, semi-synthetic penicillins were developed which initially proved effective against B-lactamase-positive Staphylococcus species. One promising example was methicillin, first used in clinical practice in 1959. However, within a year of its introduction, the first MRSA strain was reported (Jevons and others 1961).
Methicillin resistance in S aureus
Semi-synthetic penicillins such as methi cillin, oxacillin or cloxacillin contain B-lactam rings that are not hydrolysed by B-lactamases. Bacteria that are resistant to these penicillins are considered to have ‘intrinsic’ or ‘methicillin’ resistance. Resis tance is most commonly mediated by the mecA gene. A penicillin-binding protein (PBP2a) that is expressed within the bacterial cell wall is encoded for by mecA. PBP2a has a low affinity for all B-lactam antibiotics, hence bacteria that express PBP2a are unaffected (Spratt 1994). However, approximately 2 per cent of mecA - positive strains of S aureus are susceptible to methicillin, suggesting the involvement of an additional gene or genes (Niemeyer and others 1996).
The mecA gene is carried on a transposon that integrates into a single site on the staphylococcal chromosome. It has been detected in both coagulase-negative and coagulase-positive staphylococci, thus methicillin resistance is not limited to S aureus (Archer and others 1994). Some strains also possess an insertion element that enables further integration of unrelated resistant determinants (Hackbarth and Chambers 1989).
EPIDEMIOLOGY OF MRSA IN HUMANS
Hospital-acquired MRSA
MRSA is one of the major infectious control problems faced by hospitals in the UK today (Anonymous 1997, Ayliffe and others 1998, Morgan and others 2000). It currently accounts for between 30 and 40 per cent of all hospital-acquired or nosoco mial S aureus infections worldwide (Panlilio and others 1992, Lowy 1998, Anonymous 2000). Over the past 20 years, there has been a dramatic increase in the incidence of MRSA infections (Lowy 1998). Studies have shown that its detection in hospitals in the USA steadily increased from 2.4 per cent in 1974, to 29 per cent in 1991 and to 43 per cent of nosocomial infections in 2002 (Panlilio and others 1992, Collins and Tami 2003).
Early studies on MRSA demonstrated that patients in intensive care units (ICUs) are most susceptible. Contaminated ICUs can then act as reservoirs of infection, with staff or patients becoming colonised and disseminating infection throughout the hospital (Nicolle and others 1999). In turn, these patients and healthcare workers can transmit MRSA to other close associ ates and family members by direct contact.
However, in populations where MRSA is endemic, risk factors associated with true nosocomial infections (those acquired within a hospital environment) are diffi cult to discern because patients may already be colonised with MRSA when
in the hospital (Grundmann and others
2002).
Community-acquired MRSA
In recent years, the epidemiology of MRSA has changed and community- acquired infection may have become at least as important as nosocomial infection. Direct or indirect exposure to an ICU or hospital setting is now strikingly absent from many cases. Since the late 1 980s, studies have shown an increasing incidence of community-acquired MRSA in adults (Berman and others 1993, Moreno and others 1995). Initially, these cases were mainly confined to susceptible, high-risk groups of adults such as intravenous drug users (Craven and others 1986), nursing home residents (Bradley and others 1991, Muder and others 1991) and patients that were chronically ill (Boxerbaum and others 1988). However, studies from the late l990s showed an increase in community- acquired MRSA in children without any predisposing risk factors (Herold and others 1998, Frank and others 1999).
The antimicrobial susceptibility patterns of these community-acquired MRSA isolates provide further evidence of community rather than hospital origin. Unlike hospital strains, which tend to have multi- antimicrobial resistance, the community- acquired MRSA strains tend to only be resistant to B-lactam antibiotics (Adcock and others 1998, Herold and others 1998). This lack or loss of resistance suggests a community origin where antibiotic selective pressure is much lower than would be found in an ICU or hospital setting. The survival advantage of multi-drug resistance would, therefore, have less effect on the population (Adcock and others 1998, Herold and others 1998).
The origin of community-acquired MRSA remains a topic of debate. One theory is that these isolates are feral descendants of the initial hospital MRSA isolates. However, this is highly unlikely as they have distinct pulse-field gel electrophoresis (PFGE) patterns from hospital-associated
multiple antibiotics (Herold and others
1998).
Another possibility is the horizontal transfer of the methicillin-resistant gene into a formerly susceptible isolate. Penicillin resistance is readily transferred horizontally on a plasmid via transduction or conjugation. However, methicillin resistance is chromosomally encoded on a transposon via the mecA gene. Horizontal transmission of non-plasmid DNA is believed to be relatively rare. Furthermore, all the clinical strains of MRSA which have been isolated worldwide are thought to be derived from only a few ancestral strains (Kreiswirth and others 1993).
Transmission of MRSA
Colonised and infected in-patients remain the major reservoir of MRSA in hospitals, while transient carriage of the organism on the hands of healthcare workers accounts for the primary means of nosocomial infection (Thompson and others 1982). Studies have also shown that MRSA can be transmitted through direct contact in the community (Nicolle and others 1999), aerosols (Shiomorj and others 2001) and inanimate objects (Bures and others 2000). More recently, concern has been expressed that domestic pets could act as reservoirs and transmit MRSA to humans (O’Rourke 2003, Revill 2003).
EPIDEMIOLOGY OF MRSA IN DOMESTIC ANIMALS
The first documented case of MRSA infection in a domestic animal was reported in a dairy cow in 1972 (Devriese and others 1972). Since then, MRSA has been found in a variety of other domestic species including horses, chickens, dogs and cats (Cefai and others 1994, Kawano and others 1996, Hartmann and others 1997, Lilenbaum and others 1998, Gortel and others 1999, Seguin and others 1999, Tomlin and others 1999, Frank and others, Rich and Roberts 2004)
Staphylococcal species found in dogs and cats
While S aureus can be recovered from both dogs and cats, in neither species is it the most common staphylococcal strain. A variety of coagulase-positive and coagulase-negative staphylococci have been identified in dogs and cats (Scott and others 2001). The most prevalent canine isolate in the majority of studies is the coagulase-positive species Staphylococcus intermedius (Raus and Love 1983, Biberstein and others 1984, Cox and others 1984, 1988, Phillips and Williams 1984, Medleau and others 1986, Kaszanyitzky and others 2003), although a recent study in Japan reported that the coagulase-negative species Staphylococcus sciuri was most prevalent (Nagase and others 2002). Staphylococcus felis and S intermedius appear to be the most prevaentl coagulase-negative and coagulase-positive species, respectively, isolated from cats (Lilenbaum and others 1998, Pate1 and others 1999, 2002).
The frequency of S aureus carriage on the skin and mucous membranes of dogs and cats is low; isolates are generally recovered from less than 10 per cent of samples (Raus and Love 1983, Biberstein and others 1984, Phillips and Williams 1984, Medleau and others 1986, Cox and others 1988, Lilenbaum and others 1998, Patel and others 1999, 2002, Nagase and others 2002, Kaszanyitzky and others 2003). However, other studies isolated S aureus from 17 per cent of canine samples (Cox and others 1984), from 90 per cent (9/10) and 40 per cent (4/10) of healthy dogs and cats, respectively (Krogh and Kristensen 1976), and 50 per cent (16/32) of cats with pyoderma (Medleau and Blue 1988).
Methicillin-resistant
staphylococci in animals
A number of studies indicate that MRSA isolates from animals are uncommon. Two early reports were of individual cases (Cefai and others 1994, Hartmann and others 1997). The Hungarian antibiotic resistance monitoring scheme, furthermore, found that no MRSA isolates carrying the
mecA gene were obtained from animals in 2001 (Kaszanyitzky and others 2003). The authors concluded that the spread of resistant strains among different animal species and the transfer of antibiotic resistance in S aureus from animals to humans was infrequent. A recent survey in the UK also concluded that MRSA is uncommon in companion animals; of 6519 samples submitted over a 12-month period, only 95 cases of MRSA were isolated (69 dogs, 24 cats, one horse and one rabbit) (Rich and Roberts 2004).
Other reports, in contrast, have documented higher incidences of methicillin resistance. In one study of 148 samples from healthy cats, methicillin resistance was found in three of 14 S aureus isolates, eight of 26 S intermedius, six of 11 Staphylococcus simulans and five of 37 S felis isolates (Lilenbaum and others 1998). A recent study of 25 methicillin-resistant isolates from canine wounds and skin lesions reported that 23 possessed the mecA gene; nine isolates were MRSA, one was S intermedius and 15 were coagulase-negative species (10 Staphylococcus epidermidis, three Staphylococcus hominis, one Staphylococcus xylosus and one Staphylococcus haemolyticus) (Gortel and others 1999). Staphylococcus schleifrri was cultured from 15 of 40 dogs with recurrent pyoderma in another study; all nine coagulase-negative strains and two of six coagulase-positive strains were resistant to methicillin (Frank and others 2003).
These figures should be interpreted with caution. Different inclusion criteria for collection and submission may bias the apparent prevalence of MRSA and other methicillin-resistant species. Different laboratory techniques also have variable specificity and sensitivity for methicillin resistance. Traditional Kirby-Bauer disc diffusion techniques overestimate methi cillin resistance and specific broth or agar diffusion methods are preferred. PCR is the technique of choice to identify mecA (Gortel and others 1999).
The majority of MRSA infections in dogs and cats are associated with postoper ative or other wound infections, prolonged hospitalisation and/or immunosuppressive treatment: all 11 cases and 71 of 93 cases in two recent studies (Tomlin and others 1999, Rich and Roberts 2004), 11 of 14 cases at the Royal Veterinary College,
London, (Boag and others 2004), all four cases at the University of Liverpool (T. O’Neill and A. Freeman, personal commu nication) and two of three cases at North Carolina State University, College of Vet erinary Medicine (H. A. Jackson, personal communication). MRSA colonisation of the nasopharynx was found in all five cases that were sampled at the Royal Veterinary College, although it is unclear if this was present before or after the infection occurred (Boag and others 2004).
TRANSMISSION OF S AUREUS
BETWEEN HUMANS AND
ANIMALS
The idea that household pets can act as reservoirs for bacterial transmission to humans is not new. As early as 1959, S aureus was isolated from both feline and canine nostrils, and it was suggested that cats and dogs could be carriers for zoonotic staphylococcal infections in humans (Mann 1959). Another early study attributeded a high nasal carriage rate of antibiotic-resistant, coagulase-positive staphylococci in veterinary students to their exposure to hospitalised dogs that had received proophylactic antibiotics (Live and Nichols 1961). The authors suggested that prophylactic antibiotic use could result in antibiotic-resistant staphylococci becoming established in veterinary hospitals, resulting in colonisation and potentially infection of both human staff and animal patients.
A research study that introduced canine and human staphylococcal strains into canine nostrils reported that a kennel attendant became infected by one of the introduced S aureus strains (Adekeye 1981). This study concluded that a contaminated environment shared by humans and animals was likely to result in cross- contamination with staphylococci. A more recent paper reported the use of PFGE and DNA fingerprinting (amplified fragment length polymorphism) to confirm linkage of S aureus infection between humans and domestic carnivores. S aureus associated with relapsing pyoderma in a mother and daughter suffering from congenital bullous ichthyosiform erythroderma was linked to isolates from the mother’s dog and cat (Simoons-Smit and others 2000). A further report described a case of S aureus endocarditis associated with a minor dog bite (Bradshaw 2003). While these were not cases of MRSA, it does further confirm that pets can act as reservoirs for S aureus infections.
It is clear from these studies that domestic animals could acquire MRSA from humans. The potential for domestic animals to act as vehicles for MRSA transmission to humans is accepted but the clinical significance of this is less clear. The frequency of transmission between animals and humans appears to be very low, although it is possible that some cases are not investigated and, therefore, that it is under-reported. In one report, a repeated MRSA outbreak in a geriatric ward was linked with the ward cat (Scott and others 1988). The cat was not believed to have introduced MRSA but rather it had been colonised within the hospital environment and the cat had then acted as a reservoir for re-infection. Once it was removed, infectious disease control measures led to reso lution of the outbreak.
The first documented case of animal- to-human transmission was in 1994 when a husband and wife were re-infected with MRSA following initial clearance. Screening of the family dog confirmed the presence of the same MRSA strain. Treatment of the entire family group then resulted in clearance (Cefai and others 1994). Both husband and wife were nurses and the husband worked in an ICU. It is therefore likely that one or both were infected at work and originally transmitted the MRSA to the dog.
Proof of these human cases being related to those of the animal reservoirs was achieved with phage typing. This method of identification, however, has proved less reliable than PFGE in distinguishing MRSA isolates (Bannerman and others 1995). Thus the linkages can only be considered circumstantial. The first PFGE-confirmed linkage of recurrent multi-resistant MRSA infections in humans to isolates from their dog was recently reported (Manian 2003). However, it must be noted that both owners in this case were chronically ill and required frequent hospitalisation.
In most previously reported cases of canine and feline MRSA infections, either the animal itself or the owners had direct exposure to a hospital environment. How ever, of the 19 feline and canine MRSA cases seen recently at three referral institu tions, only three had owners with defini tive contact to either nursing home facilities or a hospital environment (T. O’Neill, A. Freeman and H. A. Jackson, personal communication) and most cases at one centre were considered to have been already infected at entry to the hospital (Boag and others 2004). These cases could possibly illustrate the emergence of two epidemiologically dis tinct groups (MRSA and community- acquired MRSA), as in humans. The majority of these cases, however, were associated with postoperative or other wounds, prolonged hospitalisation and/or immunosuppressive treatment and it is unclear if the infections were acquired in the community or the veterinary hospital environment.
Veterinary staff may be the primary source of infection in veterinary hospitals. One study linked MRSA infection of equine patients in a veterinary teaching hospital to nasal carriage in some of the staff, although the mode of transmission was unclear (Seguin and others 1999). It seems likely that most infections in dogs and cats are acquired from humans. Zoonotic transfer from animal to human appears to be uncommon but can occur.
The possibility that passage of an MRSA strain in another species will enhance its ability to cross the species barrier is, how ever, a concern (O’Rourke 2003).
ZOONOTIC POTENTIAL OF S INTERMEDIUS
S aureus is not the only staphylococcal species found in dogs with zoonotic potential. As mentioned previously, S intermedius is a common mucosal commensal of healthy dogs, but is also the primary pathogen in canine pyoderma (Hajek 1976, Raus and Love 1983, Biberstein and others 1984) and methicillin-resistant S intermedius has been reported in dogs and cats (Lilenbaum and others 1998, Gortel and others 1999).
S intermedius is rarely a component of the normal human bacterial flora (Talan and others 1 989b, Mahoudeau and others 1997), but it has been shown to be respon sible for canine-inflicted human bite wound infections and therefore must be classified as a zoonotic pathogen (Talan and others 1989a, Lee 1994). It has also been documented as an opportunistic pathogen causing infective endocarditis, mastoid cavity infection, catheter-related bacteraemia and pneumonia following invasive surgery (Llorca and others 1992, Vandenesch and others 1995, Gerstadt and others 1999, Kikuchi and others 2004).
Asymptomatic human carriers of S intermedius generally have intimate contact with dogs and the identified strain generally correlates with that of their pet (Goodacre and others 1997). Transmission of S intermedius between dogs suffering from deep pyoderma and their owners that resulted in asymptomatic human carriage has been demonstrated (Guardabassi and others 2004). This study also found that isolation of S intermedius from dog owners was significantly higher than from a control group. The first case of pathogenic zoonotic transmission of S intermedius was recently confirmed by 165 rRNA gene analysis of cultures iso lated from an owner’s ear infection and her dog’s natural flora (Tanner and others
2000).
S intermedius is difficult to differentiate from S aureus without specific assays. It is thus possible that some infections are incorrectly classified and that S intermedius infections in humans are under-reported.
TRANSFER OF ANTIBIOTIC
RESISTANCE BETWEEN S AUREUS AND
S INTERMEDIUS
While MRSA infection from domestic pets does not commonly appear to be a risk to human health, a greater worry would be the potential transfer of antimicrobial resistance from animal to human staphyloocccal species. Horizontal transfer of antibiotic resistance genes between human, mouse and canine staphylococcal strains occurs as frequently in vivo as in vitro (Naidoo and Lloyd 1984). Tetracycline resistance genes and structurally related plasmids of origin from human S aureus have also been identified in canine S intermedius, suggesting that genetic exchange is possible between the two species (Greene and Schwarz 1992, Schwarz and others 1998). Prudent use of antimicrobial therapy in veterinary practice should therefore be encouraged to limit the emergence of multiple antibiotic resistance in all bacterial species and reduce the risk of possible transfer of such resis tant genes to human commensal or patho genic bacteria.
CONCLUSIONS AND
RECOMMENDATIONS
MRSA and other methicillin-resistant Staphylococcus species have been identified in a variety of domestic animals, particularly dogs and cats, but the risk to human health appears to be very small. Most studies have reported a low frequency of carriage, although the data is confounded by the different selection criteria and identification techniques employed. A large scale, controlled study to ascertain the true prevalence of MRSA and other methicillin-resistant Staphylococcus species in healthy dogs and cats is urgently required. The data would allow epidemiological modelling of hospital-acquired and community-acquired MRSA in domestic animals.
The majority of MRSA infections in dogs and cats appear to be in high-risk patients and acquired by direct contact with human carriers. Human infections with MRSA and other Staphylococcus species acquired from animals are rare but using PFGE to determine linkage in suspicious cases is encouraged. Medical staff should also consider domestic pets when managing MRSA. If necessary, medical and veterinary staff should collaborate in eliminating infection from MRSA-positive households. Domestic pets in hospital environments (for example, in Pets as Therapy, and Children in Hospitals and Animal Therapy Association programmes) are of great benefit but should be routinely monitored for MRSA carriage as though they were human members of staff.
MRSA is harmless to the majority of individuals. Nevertheless, veterinary hospitals and practices should implement MRSA guidelines to minimise cross-contamination. Pet owners should be reassured they are at minimal risk but encouraged to undertake reasonable hygienic precautions. However, high-risk individuals may need extra support.
Transfer of genetic material between human and animal staphylococci is of some concern. Responsible antibiotic use to minimise the development of resistance and spread of resistance genes should be practised. A central UK database to moni tor antibiotic resistance trends in animals is desirable.
Acknowledgements
The authors are grateful to Mr Turlough
O’Neill and Dr Alistair Freeman of the
University of Liverpool, Faculty of Veteri nary Science, Miss Amanda Boag of the Royal Veterinary College, London, and Dr Hilary Jackson of North Carolina State, University College of Veterinary Medicine, for permission to quote from case material. The authors would also like to thank the British Small Animal Veterinary Associa tion Scientific Committee for its input.
References
ANON (1997) Epidemic methicillin-resistant Staphylo coccus aureus. Community Disease Report Weekly
7, 191
ANON (2000) National Nosocomial Infections Surveil lance System. American Journal of Infection Control
28, 429.448
Adcock, P. M., PASTOR, P., MEDLEY, F., PATTERSON, i. E. & MURPNY, T. V. (1998) Methicillin-resistant Staphylococcus aureus in two child care centers. Journal of Infectious Diseases 178, 577-580
ADEKEYE, i. 0. (1981) Studies on possible cross transmission of mercuric chloride resistant Staphylococcus aureus between dogs and kennel attendants. International Journal of Zoonoses 8, 72-76
ARCHER, G. L., NIEMEYER, D. M., THANASSI, J. A. & Pucci, M. J. (1994) Dissemination among staphylococci of DNA sequences associated with methicillin resis tance. Antimicrobial Agents and Chemotherapy 38,
447-454
AYLIFFE, G. A. J., BUCKLES, A., CASEWELL, M. W., COOKSON, B. 0., Cox, R. A., DUCKWORTH, G. J., FRENCH, G. L., GRIFFITH5-JoNEs, A., HEATHCOCK, R., HUMPHREYS, H., KEANE, C. T., MARPLES, P. R., SHANSON, 0. C., SLACK, P. & TEBBS, E. (1998) Revised guidelines for the con trol of methici llin-resistant Staphylococcus aureus infection in hospitals. Journal of Hospital Infection
39, 253-290
BANNERMAN, T. L., HANCOCK, G. A., TENOVER, F. C. & MILLER,
J. M. (1995) Pulsed-field gel electrophoresis as a
replacement for bacteriophage typing of Staphylo coccus aureus. Journal of Clinical Microbiology 33,
551-555
BERMAN, 0. 5., EISNER, W. & KREISWIRTH, B. (1993) Community acquired methicillin resistant Staphylococcus aureus infection. New England Journal of Medicine
329, 1896
BIBERSTEIN, E. L., JANG, S. S. & HIRSH, 0. C. (1984)
Species distribution of coagulase-positive staphylo cocci in animals. Journal of Clinical Microbiology 19,
610-615
BOAG, A., LOEFFLER, A. & LLOYD, 0. H. (2004) Methicillin resistant Staphylococcus aureus isolates from com panion animals. Veterinary Record 154, 411
BOXERBAUM, B., isco~s, M. R. & CECHNER, R. L. (1988) Prevalence and significance of methicillin resistant Staphylococcus aureus in patients with cystic fibro sis. Pediatric Pulmonology4, 159-163
BRADLEY, S. F., TERPENNING, M. S., RAMSEY, M. A., ZARINS,
L. I., JORGENSEN, K. A., S0mLE, W. S., SCHABERG, 0. R.
& KAUrFMAN, C. A. (1991) Methicillin resistant Staphy lococcus aureus: colonization and infection in a long-
term care facility. Annals of Internal Medicine ±15,
417-422
BRADSHAW, S. E. (2003) Endocarditis due to Staphylococcus aureus after a minor dog bite. Southern Medical Journal 96, 407-409
BURES, S., FISHBAIN, J. I., UYEHARA, C. F. T., PARKER, J. M. & BERG, B. W. (2000) Computer keyboards and faucet handles as reservoirs of nosocomial pathogens in the intensive care unit. American Journal of Infection Control 28, 465-471
CEFAI, C., ASHURST, S. & OWENS, C. (1994) Human carriage of methicillin-resistant Staphylococcus aureus linked with pet dog. Lancet 344, 539-540
CHAIN, E., FLOREY, H. W., GARDNER, A. D., HEATLEY, H. G.,
JENNING, M. A., ORR-EWING, J. & SANDERS, A. G. (1940)
Penicillin as a chemotherapeutic agent. Lancet 2,
226-228
COLLINS, M. & TAMI, T. A. (2003) Meth icill in-resistant Staphylococcus aureus in the practice of otolaryn gology — an emerging community acquired organ ism? Archives of Otolaryngology and Head and Neck Surgery 11, 179-183
Cox, H. U., HOSKINS, i. D., NEWMAN, S. S., FoIL, C. S., TURNWALD, 0. H. & Roy, A. F. (1988) Temporal study of staphylococcal species on healthy dogs. American Journal of Veterinary Research 49,
747-751
Cox, H. U., NEWMAN, S. S., Roy, A. F. & HOSKINS, J. D.
(1984) Species of Staphylococcus isolated from ani mal infections. Cornell Veterinarian 74, 124-135
CRAVEN, 0. E., RIXINGER, A. I., GOULARTE, 7. A. & MCCABE,
W. R. (1986) Methicillin-resistant Staphylococcus aureus bacteremia linked to intravenous drug abusers using a ‘shooting gallery’. American Journal of Medicine 80, 770-776
DEVRIESE, L. A., VANDAMME, L. R. & FAMEREE, L. (1972)
Methicillin (cloxacillin(-resistant Staphylococcus aureus strains isolated from bovine mastitis cases.
Zentralblatt fur Veterinarmedizin Riehe B 19, 59&605
FRANK, L. A., KHNIA, S. A., HNILIcA, K. A., WILKES, R. P. &
BEMIS, 0. A. (2003) Isolation of Staphylococcus
schleiferi from dogs with pyoderma. Journal of the
American Veterinary Medical Association 222, 451-
454
FRANK, A. L., MARCINAK, J. F., MANGAT, P. 0. & SCHRECKEN BERGER, P. C. (1999) Community-acquired and clindamycin-susceptible methicill in-resistant Staphy lococcus aureus in children. Pediatric Infectious Disease Journal 18, 993-1000
GERSTADT, K., DALY, J. S., MITCHELL, M., WESSOLOSSKY, M. & CHEESEMAN, S. H. (1999) Methicillin-resistant Staphylococcus intermedius pneumonia following coronary artery bypass grafting. Clinical Infectious Diseases 29, 21&219
Goodacre, R., HARVEY, R., HOWELL, S. A., GREENHAM, L. W. & NOBLE, W. C. (1997) An epidemiological study of Staphylococcus intermedius strains isolated from dogs, their owners and veterinary surgeons. Journal of Analytical and Applied Pyrolysis 44, 49-64
GORTEL, K., CAMPBELL, K. L., KAKOMA, I., WHITTEM, T., SCHA EFFER, 0. J. & WEISIGER, R. M. (1999) Methicillin resis tance among staphylococci isolated from dogs. American Journal of Veterinary Research 60, 1526- 1530
GREENE, R. I. & SCHWARZ, 5. (1992) Small antibiotic resistant plasmids in Staphylococcus intermedius. Zentralblatt fur Bakteriologi International Journal of Medical Microbiology Virology Parasitology and Infec tious Diseases 276, 380-389
GRUNDMANN, H., HORI, S., WINTER, B., TAMI, A. & AUSTIN, D. J. (2002) Risk factors for the transmission of methicillin-resistant Staphylococcus aureus in an adult intensive care unit: fittings model to the data.
Journal of In factious Diseases 185, 481- 488
GUARDABASSI, L., LOEBER, M. E. & JACOBSON, A. (2004)
Transmission of multiple antimicrobial-resistant
Staphylococcus intermedius between dogs affected
by deep pyoderma and their owners. Veterinary
Microbiology 98, 23-27
HACKBARTH, C. J. & CHAMBERS, H. F. (1989) Methicillin resistant staphylococci: genetics and mechanism of resistance. Antimicrobial Agents and Chemotherapy
33, 991-994
HAJEK, V. (1976) Staphylococcus intermedius, a new
species isolated from animals. International Journal of Systematic Bacteriology 26, 401-408
HARTMANN, F. A., TROSTLE, S. S. & KLOHNEN, A. A. 0. (1997) Isolation of methicillin-resistant Staphylo coccus aureus from a postoperative wound infection in a horse. Journal of the American Veterinary Med ical Association 211, 590-592
HEROLD, B. C., IMMERGLUCK, L. C., MARANAN, M. C., LAUDERDALE, 0. 5., GASKIN, R. E., BOYLE-VAVRA, S., LEITCH, C. 0. & DAUM, R. S. (1998) Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. Journal of the American Medical Association 279. 593-598
JEVONS, M. P., R0LIN50N, 0. N. & KNOX, R. (1961)
Celbenin-resistant staphylococci. British Medical Journal 1, 124-125
JOHN, J. F., GRIESHOP, T. J., ATKINS, L. M. & PLAIT, C. G.
(1993) Widespread colonization of personnel at a veterans affair medical center by methicillin-resistant, coagualese-negative staphylococcus. Clinical Infectious Diseases ±7, 380-388
KASZANYITZKY, E. J., .JANOSI, S., EGYED, Z., AGOST, 0. & SEMJEN, 0. (2003) Antibiotic resistance of staphylo cocci from humans, food and different animal species according to data of the Hungarian resis tance monitoring system in 2001. Acts Veterinaria Hungaria 5±, 451-464
KAWANO, J., SHIMIZU, A., SAITOH, Y., YAGI, M., SAIT0, 7. & O~Moro, R. (1996) Isolation of methicillin-resistant coagulase.negative staphylococci from chickens. Journal of Clinical Microbiology 34, 2072-2077
KIKUCHI, K., KARASAWA, T., Pi~o, C., bOA, I., HIDAI, H., YAMAURA, H., TOTsu~, K., MORIKAWA, T. & TAWAYAMA, M.
(2004) Molecular confirmation of transmission route of Staphylococcus intermedius in mastoid cavity infection from dog saliva. Journal of Infection and Chemotherapy ±0, 46-48
KIRBY, W. M. M. (1944) Extraction of a highly potent penicillin inactivator from penicillin resistant staphylococci. Science 99, 452-453
KLOOS, W. E. & BANNERMAN, T. L. (1994) Update on clinical significance of coagulase-negative staphyloccoci. Clinical Microbiology Reviews 7, 117-140
KREISWIRTH, B., KORNBLUM, J., ARBEIT, R. 0., EISNER, W., MASLOW, J. N., McGEER, A., Low, 0. E. & N0vICK, R. P.
(1993) Evidence for a clonal origin of methicillin resistance in Staphylococcus aureus. Science 259,
227-230
KROGH, H. V. & KRISTENSEN, 5. (1976) A study of skin dis eases in dogs and cats. II. Microflora of the normal skin of dogs and cats. Nordisk Veterinaermedicin
28, 459-463
LEE, 3. (1994) Staphylococcus intermedius isolated from dog bite wounds. Journal of In faction 29, 105
LILENBAUM, W., NUNES, E. L. C. & AZEREDO. M. A. I. (1998)
Prevalence and antimicrobial susceptibility of staphy lococci isolated from the skin surface of clinically normal cats. Letters in Applied Microbiology 27,
224-228
LIVE, I. & NICHOLS, A. C. (1961) The animal hospital as a source of antibiotic resistant staphylococci. Jour nal of Infectious Diseases 108, 195-204
LLORCA, I., GAGO, S., SANMARTIN, J. & SANCHEZ, R. (1992)
Infectious endocarditis caused by Staphylococcus intermedius in a patient infected with HIV. Enter medades Infecciosas y Microbiologia Clinics 10,
317-318
Lowr, F. 0. (1998) Medical progress — Staphylococcus aureus infections. New England Journal of Medicine
339. 520-532
MAHOUDEAU, I., DELABRANCHE, X., PREVOST, G., MONTEIL, H. & PIEMONT, Y. (1997) Frequency of isolation of Staphy lococcus intermedius from humans. Journal of Clin ical Microbiology 35, 2153-2154
MANIAN, F. A. (2003) Asymptomatic nasal carriage of mupirocin-resistant, methicillin-resistant Staphylo
coccus aureus (MRSA) in a pet dog associated with MRSA infection in household contacts. Clinical Infec tious Diseases 36, E26-E28
MANN, P. H. (1959) Antibiotic sensitivity testing and bac teriophage typing of staphylococci found in nostrils of dogs and cats. Journal of the American Veterinary Medical Association ±34, 469470
MEDLEAU, L. & BLUE, J. L. (1988) Frequency and antimicrobial susceptibility of Staphylococcus app isolated from feline skin lesions. Journal of the American Veterinary Medical Association 193,
1080-1081
MEDLEAU, L.. LONG, R. E., BROWN, J. & MILLER, W. H.
(1986) Frequency and antimicrobial susceptibility of Staphylococcus species isolated from canine pyo dermas. American Journal of Veterinary Research
47, 229-231
MILLIAN, S. J., BALDWIN, 3. N., RHEIN5, M. S. & WEISER, H. H. (1960) Studies on the incidence of coagulase-positive staphylococci in a normal unconfined population. American Journal of Public Health 50,
791-798
MORENO, F., CRISP, C., JORGENSEN, J. H. & PAnERSON, J. E.
(1995) Methicillin-resistant Staphylococci aureus as
a community organism. Clinical In factious Diseases
21, 1308-1312
MORGAN, M., EVANS-WILLIAMS, 0.. SALMON, R., H05EIN, I.,
LOOKER, 0. N. & HOWARD, A. (2000) The population
impact of MRSA in a country: the national survey of
MRSA in Wales, 1997. Journal of Hospital Infection
44, 227-239
MUDER, R. R., BRENNEN, C., WAGENER, M. M., VICKERS, A.,
RIH5, 3. 0., HANCOCK, 0. A., YEE, Y. C., MILLER, J. M. &
Ys, V. L. (1991) Methicillin resistant staphylococcal
colonization and infection in a long-term care facility.
Annals of Internal Medicine ±14, 107-112
NAGASE, N., SASAKI, A., YAMASHITA, K., SHIMIzU, A., WAKITA, Y., KITAI, S. & KAWANO, J. (2002) Isolation and species distribution of staphylococci from animal and human skin. Journal of Veterinary Medical Science 64, 245- 250
NAIDOO, J. & LLOYD, 0. H. (1984) Transmission of genes between staphylococci. In: Antimicrobials and Agriculture. Ed. M. Woodline. Butterworths, London. pp 285-292
NICOLLE, L. E., DYCK, B., THOMPSON, 0., ROMAN, S., KABANI, A., PLOURDE, P., FAST, M. & EMBIL, J. (1999) Regional dissemination and control of epidemic methicillin resistant Staphylococcus aureus. Infection Control and Hospital Epidemiology 20, 202-205
NIEMEYER, 0. M., PUCCI, M. 3., THANASSI, 3. A., SHARMA, V. K. & ARCHER, 0. L. (1996) Role of macA transcrip tional regulation in the phenotypic expression of
methicillin resistance in Staphylococcus aureus. Journal of Bacteriology ±78, 5464-5471
O’ROURKE, K. (2003) Methicillin-resistant Staphylococ cus aureus: an emerging problem in horses? Journal
of the American Veterinary Medical Association 223,
1399-1400
PANLILIO, A. L., CULVER, 0. H.. GAYNES, P. P., BANERJEE, S.,
HENDERSON, 7. S., TOLSON, J. S. & MARTONE, W. 3.
(1992) Methicillin-resistant Staphylococcus aureus
in US hospitals, 1975-1991. Infection Control and
Hospital Epidemiology ±3, 582-586
PATEL, A., LLOYD, 0. H., HOWELL, S. A. & NOBLE, W. C.
(2002) Investigation into the potential pathogenic ity of Staphylococcus fells in a cat. Veterinary Record
150, 668-669
PATEL, A., LLOYD, 0. H. & LAMPORT, A. I. (1999) Antimicrorbial resistance of feline staphylococci in south eastern England. Veterinary Dermatology ±0, 257- 261
PAYNE, M. C., WooD, H. F., KARAKAWA, W. & GLUCK, L.
(1965) A prospective study of staphylococcal colonization and infections in newborns and their families. American Journal of Epidemiology 82, 305-316
g/mL)
MRSA that had a pulsed-field gel electrophoresis
chromosomal pattern identical to the MRSA isolated from
the patient's nares and his wife's wound. Further
recurrence of MRSA infection and nasal colonization in
the couple was prevented only after successful
eradication of MRSA from the family dog's nares. 
and,
increasingly, community-acquired
Standard
and internal control isolates, respectively.
