Volume 51, Number 3 2010 233

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is a critically important human pathogen that is also an emerging concern in veterinary medicine and animal agriculture. It is present in a wide range of animal species, including dogs, cats, rabbits, horses, cattle, pigs, poultry, and exotic species, both as a cause of infection and in healthy carriers. Identifi ca-tion of MRSA in various species and in food has led to con-cerns about the roles of animals, both pets and livestock, in the epidemiology of MRSA infection and colonization in hu-mans. There is evidence of the role of food animals in human MRSA infections in some countries and of pets as a possible source of human infection. Some groups of individuals who work closely with animals, such as veterinarians, have high MRSA colonization rates. This article includes discussions of MRSA in human medicine, animals, and food, as well as its interspecies transmission, colonization, infection, strains, and affected populations. However, clear answers are lacking in many of these areas and limited studies may lead to premature conclusions. It is certain that animals are a source of human MRSA infection in some circumstances—but humans may also serve as sources of infection in animals. Changes in the epidemiology of MRSA in one species may be refl ected in changes in other species. The true scope of MRSA in animals and its impact on human health are still only superfi cially un-derstood, but it is clear that MRSA is a potentially important veterinary and public health concern that requires a great deal more study to enhance understanding and effective response.

Key Words: antimicrobial resistance; companion animals; livestock; methicillin-resistant Staphylococcus aureus (MRSA); zoonosis

Introduction

S taphylococcus aureus is a Gram-positive bacterium and important opportunistic pathogen in various spe-cies. Historically it has been a leading cause of both

skin and invasive infections in humans, and its impact is no less today. One reason for the continuing important role of S. aureus in disease is its propensity to become resistant to antimicrobials. The introduction of penicillin had a profound effect on staphylococcal infections, but penicillin resis-tance soon followed. Similarly, after the introduction of new antimicrobials such as methicillin, it was not long before methicillin-resistant S. aureus (MRSA1) developed.

Methicillin resistance is conferred by the mecA gene, which encodes for production of an altered penicillin bind-ing protein (PBP2a or PBP2') that has a low affi nity for all beta-lactam antimicrobials (penicillins, cephalosporins, car-bapenems), rendering staphylococci resistant to this large and critical antimicrobial class. Frequently, MRSA isolates are also resistant to other antimicrobial classes, further limiting treatment options.

MRSA in Human Medicine

When MRSA emerged in international hospitals in the 1960s, there was initially limited concern because of the relatively low incidence of disease. It was not until the late 1970s and early 1980s that MRSA rates in hospitals increased dramati-cally, starting a “pandemic” phase (Chambers and DeLeo 2009). MRSA had (and continues to have) a tremendous impact on morbidity and mortality in hospitals, but another major epi-demiological shift occurred in the 1990s with the widespread emergence of community-associated MRSA (CA-MRSA1) infections.

Early reports of CA-MRSA were associated with strains most commonly found in hospitals and typically involved people with prior healthcare exposure and other healthcare-associated risk factors. Subsequent reports described infec-tions (sometimes fatal) in people with little to no healthcare contact or other recognized risk factors (Diederen and Kluytmans 2006; Frazee et al. 2005a,b). These infections were often associated with strains different from those that predominated in healthcare facilities, demonstrating a unique community-associated disease, not a hospital-associated infection. Now MRSA is a leading cause of community-associated skin and soft tissue infections in some regions, with rare but dramatic serious infections such as necrotizing

1Abbreviations used in this article: CA-MRSA, community-associated MRSA; MRSA, methicillin-resistant Staphylococcus aureus; ST, sequence type

J. Scott Weese

J. Scott Weese, DVM, DVSc, DACVIM, is an associate professor in the Department of Pathobiology at the University of Guelph’s Ontario Veterinary College in Ontario, Canada.

Address correspondence and reprint requests to Dr. J. Scott Weese, Department of Pathobiology, University of Guelph, Guelph, Ontario N1G 2W1, Canada or email jsweese@uoguelph.ca.

Methicillin-Resistant Staphylococcus aureus in Animals

234 ILAR Journal

fasciitis and necrotizing pneumonia (Frazee et al. 2005a,b; Miller et al. 2005).

MRSA in Animals

It is perhaps not surprising that MRSA has emerged in a va-riety of animal populations, apparently through different mechanisms. The close contact between humans and various animal species creates the potential for exposure of animals to “human” organisms, and antimicrobial use in animals pre-sumably facilitates the emergence and spread of MRSA. But mechanisms, risk factors, and other information about the emergence of MRSA in animals are rather poorly under-stood at this point, as repeatedly illustrated in the following discussions.

Household Pets

Exposure of household pets to MRSA was probably inevi-table as the prevalence of CA-MRSA increased in humans. At least one study has demonstrated that concurrent colo-nization of people and their pets with indistinguishable methicillin-susceptible S. aureus (MSSA) strains is not un-common (Hanselman et al. 2009), indicating the potential for transmission of MRSA between people and pets in a household.

Prevalence

An understanding of the dynamics of S. aureus colonization in dogs and cats is limited, but it is clear that the bacterium can cause opportunistic infections or reside in the nasal pas-sages or intestinal tract of healthy humans and animals. As in many other species, MRSA is present in a small percentage of healthy dogs and cats. Prevalence data are variable and comparison between studies is inadvisable because of dif-ferent populations and methods, but most canine and feline population-based studies have reported rates of 0-4% (Abraham et al. 2007; Baptiste et al. 2005; Boost et al. 2007b; Griffeth et al. 2008; Hanselman et al. 2007; Kottler et al. 2008; Loeffl er et al. 2005; Vengust et al. 2006). Rates may be higher in studies of focal populations—for example, 9% in dogs at a veteri-nary clinic with reported MRSA cases and 7.8% in dogs at a rescue shelter (Loeffl er et al. 2005, 2010). But colonization of dogs and cats appears to be transient, as most eliminate the pathogen naturally within a few weeks (Lefebvre et al. 2009; Loeffl er et al. 2010).

Colonization and Infection

There have been few studies of the risk factors for MRSA colonization, although one showed that living with a human healthcare worker was associated with colonization of dogs (Boost et al. 2007b). Colonization of pets is of concern for two reasons: (1) colonized pets are presumably at increased

risk of developing an MRSA infection, although proof of this is currently lacking, and (2) they may be a source of hu-man infection, as discussed below.

While most animals with MRSA are merely colonized, a wide range of clinical infections can occur. As would be ex-pected with staphylococci, most MRSA infections in pets affect the skin and soft tissue. Wound infections, surgical site infections, pyoderma, otitis, and urinary tract infections are most common, but various other opportunistic infections have been reported (Baptiste et al. 2005; Griffeth et al. 2008; Leonard et al. 2006; Morris et al. 2006a,b; Tomlin et al. 1999; Vitale et al. 2006; Weese et al. 2006b). One study cited the administration of antimicrobials, particularly fl uoroqui-nolones, as a risk factor for MRSA (versus MSSA) infection in dogs and cats (Faires et al. 2009).

Strains

Typing data provide insight into the epidemiology of MRSA in pets and its relationship to humans. MRSA strains in pets tend to closely refl ect those in people in any given region (Baptiste et al. 2005; Grinberg et al. 2008; Leonard et al. 2006; Malik et al. 2006; Moodley et al. 2006; O’Mahony et al. 2005; Strommenger et al. 2006; Weese et al. 2006b). For example, the USA100/CMRSA-2 clone, the predomi-nant strain in colonized humans (Tenover et al. 2008), is commonly reported in pets in North America (Lefebvre et al. 2009; Weese et al. 2006b, 2007). Results are similar in the United Kingdom, but with different strains, as eMRSA-15 and -16 predominate there in both people and pets (Loeffl er et al. 2005, 2010; Moodley et al. 2006). These fi ndings pro-vide much support to the hypothesis that MRSA in pets is ultimately human in origin. Recently, however, there have been reports of MRSA infections in dogs caused by sequence type (ST1) 398, a clone associated with food animals and an emerging cause of human CA-MRSA in some regions (Nienhoff et al. 2009; Witte et al. 2007). Whether this repre-sents an uncommon occurrence or the emergence of a new concern in pets is unclear.

Pet Therapy Animals

Animals (predominantly dogs) that participate in pet therapy programs raise unique concerns about the risks of interspecies transmission (Lefebvre et al. 2009). A recent article cited healthcare center visitation and contact with children during organized pet therapy sessions as risk factors for MRSA colonization of dogs: animals that were allowed to lick pa-tients or that received treats from them were at higher risk of MRSA acquisition (Lefebvre et al. 2009), possibly through oral exposure to the pathogen on patients’ skin. Another po-tential concern with pet therapy animals is their possible transient contamination by MRSA in the absence of coloni-zation or infection (Enoch et al. 2005; Lefebvre and Weese 2009). One study demonstrated that petting could lead to the transfer of MRSA applied to a dog’s coat (in the absence of

Volume 51, Number 3 2010 235

the animal’s or person’s known contact with an infected or colonized individual) (Lefebvre and Weese 2009).

Horses

There are some interesting parallels between MRSA in horses and household pets, but also some remarkable differences. As with pets, the fi rst reports of MRSA in horses involved sporadic infections or small clusters and the belief that these were unusual events involving direct transmission from humans (Hartmann et al. 1997; Seguin et al. 1999; Shimizu et al. 1997). Also as with pets, subsequent investigation iden-tifi ed colonization of a small percentage of healthy horses. Most studies report colonization in 0-11% of horses on farms or upon admission to veterinary hospitals (Anderson and Weese 2007; Baptiste et al. 2005; Burton et al. 2008; Van den Eede et al. 2009; van Duijkeren et al. 2010; Vengust et al. 2006; Weese et al. 2005b, 2006c), but there may be higher rates in specifi c groups (e.g., 43% on one farm; Weese et al. 2005b).

Risk Factors for Colonization and Infection

Reports indicate that antimicrobial exposure is a risk factor both for being colonized with MRSA on admission to an equine hospital and for becoming colonized during hospital-ization (Weese and Lefebvre 2007; Weese et al. 2006c). Other risk factors for colonization upon hospital admission include previous colonization of the horse, previous identifi cation of colonized horses on the farm, admission to the neonatal in-tensive care unit, and admission to a service other than sur-gery (Weese and Lefebvre 2007). Broader study is required to identify true causal risk factors, particularly those that might be modifi able or avoidable.

Most colonized horses do not develop clinical infections, but colonization at the time of hospital admission is a risk factor for the development of such infections (Weese et al. 2006b). MRSA-colonized horses are also of concern because of the potential for transmission to other horses, humans, and potentially other animal species.

Strains

As with dogs and cats, MRSA colonization in horses appears to be transient in most cases, and decolonization occurs nat-urally in the absence of reinfection (Weese and Rousseau 2005). One clear difference between MRSA in horses and household pets is the strains that tend to be involved. Most initial reports of MRSA in horses involved ST8 or related (i.e., ST254) strains, especially the USA500/CMRSA-5 clone in North America (Anderson and Weese 2007; Cuny et al. 2006; Moodley et al. 2008; O’Mahony et al. 2005; Weese et al. 2005a,b). These are human epidemic clones but they are cur-rently uncommon in people (Christianson et al. 2007), so their prevalence in horses is disproportionate, suggesting that

this strain may be more adept than others at survival in horses. Other common human epidemic clones (e.g., USA100/CMRSA-2) occur in horses, albeit much less frequently (Weese et al. 2005a,c), and recent reports cite ST398 in horses in Europe and Canada (Cuny et al. 2008; Tokaletoff et al. 2009; Van den Eede et al. 2009; van Duijkeren et al. 2010; Walther et al. 2009). Although equine MRSA surveil-lance has been limited in the past in most areas, it is possible that this documented incidence truly represents the emer-gence of ST398 in those populations rather than previously undiagnosed endemic infection.

Sources and Transmission

It is likely that there are different origins of MRSA, sources of infection, and routes of transmission in the horse popula-tion, where ST8 strains (ultimately human in origin) may be horse adapted and endemic, sporadic infection may be the result of more common human epidemic clones (as is the situation in pets), and ST398 may have originated from food animals, as discussed below.

Clinical MRSA infections can occur as outbreaks but sporadic infections are most common, both in veterinary hospitals and in the community, where they may be accom-panied by a wide range of opportunistic infections. Joint, incision, and skin/soft tissue infections are most common in community-onset cases, and surgical site infections predom-inate in hospitalized horses (Anderson et al. 2009; Hartmann et al. 1997; O’Mahony et al. 2005; Seguin et al. 1999; Weese et al. 2005a). Other possible infections include pneumonia, metritis, omphalophlebitis, sinusitis, bloodstream infection, invasive device infection, osteomyelitis, tenosynovitis, metritis, and mastitis (Anderson et al. 2009; Baptiste et al. 2005; Cuny et al. 2006; Middleton et al. 2005; Shimizu et al. 1997; Weese et al. 2005a). The severity of disease can be quite variable, from mild and superfi cial to aggressive and life-threatening, and there is no evidence that MRSA infections have a different clinical presentation or outcome than MSSA infections (Anderson et al. 2009a). Risk factors for MRSA infection have not been reported, as opposed to studies in-volving colonization.

Food Animals

The emergence and dissemination of MRSA in food animals (livestock-associated MRSA) appear to have taken a different course from that in companion animals. Rather than emerg-ing from human sources, MRSA seems to have evolved independently in one or more food animal species, with sub-sequent dissemination and interspecies transmission.

Cattle

Following the initial report of MRSA in a dairy cow in 1972 (Devriese et al. 1972), sporadic cases of MRSA mastitis in

236 ILAR Journal

dairy cattle were described, typically at a low prevalence, among S. aureus isolates from clinical or subclinical mastitis. Notwithstanding more recent reports (Juhász-Kaszanyitzky et al. 2007; Kwon et al. 2005; Lee 2003, 2006; Moon et al. 2007), the incidence of MRSA mastitis and the prevalence of methicillin resistance among bovine S. aureus isolates appears to be quite low (Kwon et al. 2005; Lee 2003), so MRSA does not appear to be a common or important bovine mastitis patho-gen at this time. The long-term low prevalence of MRSA mastitis is quite surprising given the number of years since the fi rst identifi cation of MRSA in cattle and the close con-tact of humans with the udders of dairy cattle.

Minimal information is available about MRSA coloni-zation of healthy cattle. A recent Dutch study found 28% of veal calves colonized with MRSA (Graveland et al. 2008), but in Switzerland the pathogen was isolated from only 1.3% of calves and 0.4% of adult cows (Huber et al. 2009) and in Canada from none of 491 Canadian feedlot cattle (Weese et al. 2009b). Clearly, more study of healthy cattle is required.

Pigs

Signifi cant concerns about MRSA and food animals emerged in just the past 5 years after an alarming report about infec-tions and high rates of colonization among Dutch pig farm-ers. An intensive international investigation of MRSA in food animals, predominantly pigs, followed reports of both “unexpected” CA-MRSA infections in people in the Nether-lands who had been in contact with pigs and an exception-ally high colonization rate of pig farmers—760 times that of the general Dutch population (Voss et al. 2005).

A unique characteristic of the Dutch report was that the human isolates and one from a pig were nontypable by smaI pulsed fi eld gel electrophoresis (PFGE) and were ST398, a historically rare clone. This led to further studies of MRSA colonization in pigs, both in the Netherlands (de Neeling et al. 2007; Huijsdens et al. 2006; van Duijkeren et al. 2008) and elsewhere, including Belgium (Dewaele et al. 2008), Canada (Khanna et al. 2007), Germany (Witte et al. 2007), Singa-pore (Sergio et al. 2007), and the United States (Smith et al. 2008b). But the resulting prevalence data are quite variable between farms—from 0 to 100%—and comparisons of the data are inadvisable because of differing study populations (ages, pig production systems) and methods. The main con-clusion should be that MRSA is prevalent among pigs in many countries.

Because ST398 strains have predominated in reports of MRSA in pigs internationally (e.g., de Neeling et al. 2007; Dewaele et al. 2008; Hasman et al. 2010; Khanna et al. 2007; Sergio et al. 2007; Smith et al. 2008a; van Duijkeren et al. 2008), it is plausible that this strain emerged in pigs and was subsequently disseminated to other species. The fi nding of methicillin-susceptible ST398 in pigs (Guardabassi et al. 2007) supports this hypothesis, although proving it retrospectively is diffi cult. Other strains have also been identifi ed. Common

human epidemic clones are present in pigs in some regions (e.g., the USA100/CMRSA-2 in Canada; Khanna et al. 2007). While it is not possible to draw defi nitive conclusions, it is most likely that this represents human-to-pig transmission. Studies of pigs in China also report an unrelated clone, ST9, the source and implications of which are unknown (Cui et al. 2009; Wagenaar et al. 2009).

Risk factors for MRSA colonization of pigs have not been adequately investigated. Tetracycline resistance is typ-ical in ST398 and has led to the assumption that the emer-gence of this strain resulted from heavy tetracycline use in pig production (de Neeling et al. 2007). However, such con-clusions may be misleading—tetracycline resistance is also very common in equine ST398 and CMRSA-5/USA500 isolates (Van den Eede et al. 2009; Weese et al. 2005a) despite the sparing use of tetracycline in horses. MRSA is also present on antibiotic-free swine farms (Weese et al. 2009c).

Intuitively, it is reasonable to hypothesize that antimicro-bial use on farms would drive the emergence and dissemina-tion of MRSA, but available data are inadequate. A recent study described an increase in the prevalence of colonization among a small group of pigs after tetracycline administra-tion (van Duijkeren et al. 2008), but the increase was not statistically signifi cant and other factors may have been in-volved. In that study, MRSA colonization was present in pigs at 1 out of 21 farms that did not routinely administer antimicrobials versus 6 out of 10 farms that did. Larger stud-ies are needed to determine the true role of antimicrobials in MRSA in pigs and to differentiate the role of antimicrobials versus other management factors in differences in MRSA rates between farms.

Despite the high prevalence of colonization in pigs, clinical infections are rare, with only sporadic reports of exuda-tive dermatitis, urinary tract infection, and mastitis-metritis-agalactia syndrome (Schwarz et al. 2007; van Duijkeren et al. 2007). The potential impact of MRSA in pigs is there-fore greater from a public health standpoint, as discussed below, than an animal health standpoint.

Poultry

There have been few investigations of MRSA in poultry. Two reports describe MRSA isolation from healthy and sick chickens (Lee 2003, 2006), but there are limited prevalence and incidence data. Two recent studies reported isolation of ST398 from healthy chickens (Nemati et al. 2008; Persoons et al. 2009), and a third, involving characterized isolates from infected poultry, reported the predominance of a com-mon human epidemic clone (clonal complex 5) (Hasman et al. 2010). Whether the presence of different strains in studies reporting infection versus colonization indicates dif-ferences in the strains that cause colonization versus infec-tion or regional differences in MRSA distribution is unclear. More study of poultry is required to determine the epidemi-ology of infection and colonization.

Volume 51, Number 3 2010 237

Interspecies Transmission of MRSA: Affected Populations

There is clear evidence that MRSA can be transmitted be-tween humans and animals, in both directions, yet the fre-quency, direction, and overall relevance have not been clearly established, and the roles of different animal species in the transmission of MRSA to humans are very superfi cially understood.

Household Pets

Some of the earliest public health concerns about MRSA and animals focused on household pets. Given the close con-tact of many people and their pets and the sheer number of pets, this concern is reasonable. Numerous studies report the concurrent isolation of indistinguishable MRSA strains from people and pets (predominantly dogs and cats) in the context of the colonization of both pets of MRSA-infected people and people whose pets are infected (Boost et al. 2007a; Faires et al. 2009; Leonard et al. 2006; Loeffl er et al. 2005; Manian 2003; Moodley et al. 2006; O’Mahony et al. 2005; Sing et al. 2008; van Duijkeren et al. 2005; Weese et al. 2006b). How-ever, cross-sectional evaluation of these colonizations cannot determine the direction of transmission nor rule out common-source infection. Pets have been implicated as the cause of human infections (Manian 2003; Sing et al. 2008), but it’s debatable whether pets can truly be implicated in such cases. Finding the same strain in a person and a pet certainly sug-gests interspecies transmission, but identifying an individual as the cause of infection using single cross-sectional investi-gation is not reliable: MRSA strains in pets are typically those most common in people, so determination of strain type provides no information about the potential origin of infection.

There is currently no evidence indicating that the general pet-owning population is at increased risk of MRSA infec-tion or colonization, but there has been minimal study of this area. However, a study of Canadian and American house-holds with a MRSA-infected pet found colonization of 18% of the humans (Faires et al. 2009), a rate much higher than the 1-3% estimated for the general population in that region (Gorwitz et al. 2008; Hanselman et al. 2008). Thus, it is rea-sonable to assume that exposure to an infected animal is a risk factor for MRSA colonization of owners, with unknown clinical relevance.

Particular attention has been paid to households with re-current MRSA infections in humans. Case reports have de-scribed isolation of MRSA from pets in such households (Faires et al. 2009; Manian 2003; Sing et al. 2008), but care must be taken when interpreting the relevance of case re-ports. In one small prospective study, MRSA was isolated from pets in only one out of eight households (13%) with recurrent MRSA infections (Faires et al. 2009). While that study was quite small and further investigation is needed, it is important to note the low prevalence and the fact that in

the only household with colonized pets, there was also a colonized healthy person. The presence of MRSA in a pet does not necessarily indicate that the animal was or could be a source of human infection, although concerns should not be dismissed.

In summary, current data strongly suggest that MRSA can move between people and pets in households, whether the individuals are colonized or infected. Research is needed to understand the frequency of this cross-species transmis-sion and its risk to animal and human populations.

Horses

There is clear evidence of interspecies transmission of MRSA between horses and humans, resulting in both colo-nization and infection. Higher rates of MRSA colonization than would be expected have been identifi ed in horse owners and equine veterinarians. One study reported colonization of 13% of horse owners and the presence of a colonized person on every farm that had one or more colonized horses, with indistinguishable human and equine strains (Weese et al. 2005b). The prevalence in that study should be interpreted with caution because a subset of farms was chosen based on previous diagnosis of MRSA on the farm, and the true popu-lation prevalence among horse owners is unknown. Studies of veterinary personnel have also strongly suggested an oc-cupational risk of horse contact, as discussed below.

Laboratory Animals

The potential for colonization, amplifi cation, and interspe-cies transmission of MRSA should be of concern for people involved with laboratory animal colonies. The mixing of ani-mals, use (and potential overuse) of antimicrobials, use of invasive devices and implants, and contact with humans all create a clear opportunity for introduction and transmission of MRSA.

There are very few reports of MRSA infection or colo-nization in laboratory animal colonies,2 but this may simply be a refl ection of the uncommon publication of MRSA in-fections in such facilities. Anecdotally, outbreaks of MRSA infection and colonization in laboratory animals, especially nonhuman primates, are not uncommon but are rarely re-ported in the literature. This author has been contacted nu-merous times about MRSA infections in research animals, none of which have ever been published. This understand-able reluctance to publicize infections, given sensitivities regarding management of research animals and the high-profi le nature of MRSA, complicates assessment of the scope of the problem, risk factors, and ways to prevent or control infections.

2Two exceptions are MRSA pneumonia in a rhesus macaque at a research facility (Rivas et al. 2007) and ST398 MRSA colonization of pigs used in research (Sergio et al. 2007).

238 ILAR Journal

One retrospective study identifi ed MRSA infections of intravenous catheters in two rhesus macaques (Macaca mulatta; Taylor and Grady 1998), but there was no apparent further investigation or characterization of the MRSA isolates. In-fections of invasive devices, particularly those that are left in place for prolonged periods of time, may pose a high risk. Sporadic cases or outbreaks raise concerns about animal health, the need for device/implant removal, costs of treatment, and the potential for zoonotic transmission.

The risk of MRSA in laboratory animal facilities is not restricted to those with active MRSA research programs. Certainly, the presence of experimentally infected animals in a facility could increase other animals’ risk of exposure, whether from colonized animals, environmental contamina-tion, fomites, or colonized personnel. However, considering the prevalence of MRSA in the general population and the potential for higher rates of carriage in animal care person-nel, exposure of laboratory animals from colonized humans probably poses the greatest risk. Routine infection control and surveillance activities must address the ever-present risk of introduction of MRSA into a facility.

Food Animals

Livestock-associated MRSA has emerged as a pressing con-cern in some countries. Since the fi rst reports of human in-fections associated with MRSA in pigs, subsequent studies have confi rmed that pig contact is a risk factor for MRSA infection and colonization (Lewis et al. 2008; van Rijen et al. 2008). The studies have largely focused on the role of pigs in the Netherlands, with less information about other food ani-mals and other regions.

There have been dramatic increases in human ST398 in-fection and colonization in the Netherlands, where the prev-alence of PFGE nontypable (and therefore presumed ST398) MRSA isolates recovered from humans rose from 0% in 2002 to more than 21% in 2006 (van Loo et al. 2007a). Changes in surveillance likely accounted for some of this increase, but it is clear that ST398 rates are rising and are to

a large degree associated with animal contact, as colonization rates have been particularly high in various groups with live-stock contact, such as veterinarians (discussed in the next sec-tion), farmers, and people living on farms (Table 1). Specifi cally, contact with pigs or cattle is a risk factor for ST398 or non-typable MRSA colonization (Köck et al. 2009; van Loo et al. 2007a; van Rijen et al. 2008; Vandenbroucke-Grauls and Beau-jean 2006): studies reported colonization in 32% of people with veal calf contact in the Netherlands (Graveland et al. 2008) and in 32% of hospitalized people who had contact with pigs and veal calves (van Rijen et al. 2008). These rates them-selves are remarkable, but they are astounding considering that the prevalence of colonization in the general Dutch population is less than 1% (Wulf et al. 2008).

A recent Dutch study indicated that the annual incidence of MRSA increased more than threefold from 2001 to 2006 and that this increase was entirely attributable to animal- related MRSA (van Rijen et al. 2009). According to the study, animals accounted for 26% of the cases in people who were identifi ed as colonized upon hospital admission. Because of the risk associated with pig contact, Dutch hospitals have ad-opted strict MRSA control measures, and a Dutch report rec-ommended that people with pig contact be isolated at the time of their hospital admission until MRSA screening results are available (Vandenbroucke-Grauls and Beaujean 2006).

Farm-based risk factors for MRSA acquisition have been only minimally investigated. Not surprisingly, working in barns with colonized pigs is a risk factor (van den Broek et al. 2008), and more intensive and longer contact is prob-ably an important factor, as evidenced by transient MRSA carriage in people who visit farms to collect samples versus higher rates of colonization in workers with more intensive or longer contact (van den Broek et al. 2008).

The geographic variation in the prevalence of ST398 colonization and incidence of infection in humans is quite interesting. Although it is a leading cause of CA-MRSA in-fection in some European countries, ST398 MRSA infec-tions are currently rare in North America, where, despite the presence of ST398 in livestock, there are very few reported infections in humans (Golding et al. 2009). The reason for

Table 1 Methicillin-resistant Staphylococcus aureus (MRSA) colonization in humans who have contact with food animals

Study population Countrya Prevalence Reference

Swine farm personnel Belgium 38% Denis et al. 2009

Swine farm personnel United States 37% Harper et al. 2009

People with veal calf contact The Netherlands 32% Graveland et al. 2008

Hospitalized people with pig or veal calf contact

The Netherlands 32% van Rijen et al. 2008

People working and living on pig farms

The Netherlands 30% van den Broek et al. 2008

Swine farm personnel Canada 20% Khanna et al. 2007

aCountry where sampling was performed. Some individuals may have been from other countries.

Volume 51, Number 3 2010 239

this is unclear. Various possibilities exist, including differ-ences in direct and indirect contact with food animals, much lower population density in North American pig-rearing re-gions, and the more common presence of other (perhaps competing) MRSA strains in people in the general popula-tion. Another possibility is that this is an emerging disease in North America, with a later onset than in Europe.

Veterinary Personnel

It has become clear that MRSA exposure is an occupational risk in veterinary medicine. Most, but not all, studies of colo-nization of veterinary personnel have indicated relatively high colonization rates (Table 2). While these studies have typically not involved a non-animal-contact control group, the reported prevalences have tended to be well in excess of those for the general population, strongly suggesting an in-creased risk of exposure.

The strains present in veterinary personnel further support the hypothesis of occupational exposure, at least for equine and food animal veterinarians. Studies of the former have predominantly identifi ed ST8 (or related) strains (Anderson et al. 2008; Cuny et al. 2006, 2008; Hanselman et al. 2006; Moodley et al. 2006; O’Mahony et al. 2005; Weese et al. 2005a,b), suggesting an equine origin because of the rela-tive rarity of these strains in the general human population (Christianson et al. 2007). Similarly, studies of swine veterinar-

ians and farmers have reported predominantly ST398 strains, supporting occupational exposure (Huijsdens et al. 2006; Khanna et al. 2007; Smith et al. 2008a; Wulf et al. 2008).

Studies of small animal veterinary personnel have reported predominance of common human epidemic clones (Burstiner et al. 2009; Hanselman et al. 2006; O’Mahoney et al. 2005), as would be expected based on the strains most commonly found in pets. That fi nding complicates determination of likely origin of colonization. Other studies of this group have reported relatively low rates of colonization, similar to or only slightly higher than expected for the general population (Hanselman et al. 2006; Wulf et al. 2006; Zemlicková et al. 2009). In contrast, a recent study of people attending a vet-erinary surgery conference in the United States reported 17% colonization of small animal veterinary personnel, a rate that was no different from equine personnel (Burstiner et al. 2009). This could represent inherent differences in study popula-tions but could also indicate a true increase in MRSA in small animal veterinary personnel, a possibility that requires further investigation.

Factors associated with MRSA colonization in veterinary personnel have not been thoroughly investigated. One study of equine veterinarians identifi ed hand hygiene as an impor-tant protective factor: veterinarians who reported that they regularly washed their hands between farms and after handling potentially infectious cases had signifi cantly lower coloniza-tion rates (Anderson et al. 2008), a clear indication of the usefulness of routine hand hygiene. A previous diagnosis of

Table 2 Methicillin-resistant Staphylococcus aureus (MRSA) colonization in veterinary personnel

Study population Countrya Prevalence Reference

Small animal veterinary clinic staff

United Kingdom 18% Loeffl er et al. 2005

Veterinary surgery conference attendees

United States 17% Burstiner et al. 2009

Large animal veterinarians United States 15.6% Hanselman et al. 2006

Equine veterinary hospital personnel

Canada 14% Weese et al. 2005a

Horse owners and veterinarians

United States and Canada 13% Weese et al. 2005b

Swine veterinary conference attendees

The Netherlands 12.5% Wulf et al. 2007

Veterinary technicians United States 12% Hanselman et al. 2006

Equine veterinarians United States 10.1% Anderson et al. 2008

Veterinarians and veterinary students with livestock contact

The Netherlands 4.6% Wulf et al. 2006

Small animal veterinarians United States 4.4% Hanselman et al. 2006

Veterinarians Denmark 3.9% Moodley et al. 2008

Veterinarians Czech Republic 0.7% Zemlicková et al. 2009

aCountry where sampling was performed. Some individuals may have been from other countries.

240 ILAR Journal

MRSA (infection or colonization) or treatment of a horse with MRSA were both associated with MRSA colonization in that study (Anderson et al. 2008).

There are limited reports of zoonotic infections in veteri-nary personnel, but it is not known whether that indicates a low incidence of disease or underreporting. In one case a veterinarian working with an infected horse acquired a tattoo-site infection (Weese et al. 2005a). In another instance, an outbreak of MRSA skin infections occurred in three people, wearing gloves and coveralls, who worked with a colonized newborn foal over a 4-hour period to provide general nursing care in a neonatal intensive care unit (Weese et al. 2006a). Overall, 19% of people that had similar contact with the foal were infected or colonized.

Given reports of zoonotic infections and the apparent high incidence of colonization of some veterinary groups, MRSA should be considered an occupational risk in veterinary medicine.

MRSA in Food

Considering the increasing evidence of MRSA in food ani-mals, it is logical that concerns would emerge about MRSA contamination of food and to assume that colonized animals were the source of contamination. But this connection has yet to be clearly demonstrated. ST398 MRSA has predomi-nated in some, but not all, reports of MRSA in meat. Studies have reported the presence in meat of strains more com-monly found in people, including strains not yet reported in food animals (Lozano et al. 2009; Pu et al. 2009; Weese et al. 2009a), raising questions about whether contamination is from food animals, other sources such as people involved in food processing, or both. Clearly, more information is required, necessitating research beyond the cross-sectional study of retail food contamination.

It is also reasonable to suspect that MRSA food poison-ing could become more common with an increase in food contamination and colonization of food handlers. As with methicillin-susceptible staphylococci, classical staphylococ-cal “food poisoning” caused by ingestion of preformed en-terotoxins can occur. While MRSA isolates can possess various enterotoxin genes there is only one report of staphy-lococcal food poisoning caused by MRSA (Jones et al. 2002). This may be in part because of limited attempts to culture stool for S. aureus in cases of suspected food poisoning. Clinically, food poisoning caused by MRSA should be no different from that caused by MSSA, but MRSA-contami-nated food could also be a source of intestinal colonization.

In addition to these risks, food may be a concern as a vehicle of MRSA extraintestinal colonization and infection. Contaminated food was implicated as a source of an out-break in a hospital in the Netherlands, where MRSA was isolated from a banana peeled by a colonized food preparer (Kluytmans et al. 1995). Based on that fi nding and the lack of another identifi ed route of transmission, food was sus-pected as being a vehicle for MRSA, although defi nitive

proof was lacking. It is certainly plausible that surface con-tamination of food could lead to colonization if people touch their noses after contaminating their hands. Infection of hand wounds could also be a concern, but neither of these has been proven.

Recent attention has largely focused on contamination of meat, based on the presence of MRSA in food animals and on reports of MRSA-contaminated retail meat, involving a range of meat products and with prevalences ranging from 0.4% to 12% (de Boer et al. 2009; Lin et al. 2009; Lozano et al. 2009; Pu et al. 2009; van Loo et al. 2007b). Although it is not advisable to compare prevalence data because of varying methods, sample collection schemes, and sample types, these studies indicate that MRSA is present in a varying but generally small percentage of retail meat samples. The use—or not—of enrichment culture methods, for example, can result in differing data, because very low levels of contamination are detectable in the culture. A Canadian study identifi ed MRSA in 6.3% of ground pork and 5.6% of ground beef, yet 32% and 45% of positive pork and beef samples, respectively, had up to 20 CFU/g; most quantifi able samples had fewer than 100 CFU/g and the highest had 3590 CFU/g (Weese et al. 2009a). While the potential infective dose is completely un-known, it is reasonable to assume that low levels of MRSA are of less concern than higher levels, but it is nonetheless important to consider low levels when evaluating the poten-tial of food as a source of infection.

Despite increases both in MRSA food contamination and in human incidence of CA-MRSA and ST398 infections, there are no reports of a direct link between the two. There is no question that food can be contaminated with MRSA, and a role in human disease can be hypothesized, but no objective data are available to support or refute such a hypothesis. More intensive surveillance and the inclusion of queries about food exposure (ingestion and contact) in CA-MRSA investi-gations are necessary to elucidate the true role of food in human disease. Even so, determination of an association may be diffi cult, since infection occurs only in certain situa-tions and often well after exposure.

Conclusions

The overall role of animals in human MRSA infections varies tremendously between animal species and regions. And be-cause the epidemiology of MRSA in animals is only superfi -cially understood, it is inappropriate to draw conclusions or take actions based on rather limited data. However, it is clear that MRSA is an excellent example of the “One Health” concept as it can reciprocally affect human and animal populations.

Concerns about MRSA in animals are reasonable and require careful study of various aspects to better understand the emergence and dissemination of MRSA in different spe-cies and to characterize interspecies transmission. At the same time, it is important to remember that a minority of human MRSA infections are directly associated with animals. Thus,

Volume 51, Number 3 2010 241

a balanced approach is key in efforts to reduce the implica-tions of MRSA in both animals and humans while avoiding an excessive response that might unnecessarily harm human interactions with pets, food animals, and food.

As MRSA becomes (or has become) established in dif-ferent animal and human populations, elimination of all risk will be impossible. However, proper study of MRSA in ani-mals, characterization of interspecies transmission, identifi -cation of true human and animal health risks, and development of evidence-based control measures can surely reduce the impact on animal health and welfare, human health, agricul-ture, and the human-animal bond.

Acknowledgments

The author’s MRSA research is funded by the Canadian In-stitutes of Health Research, Public Health Agency of Canada, Ontario Veterinary College Pet Trust, Canadian Pork Council, National Pork Board, Beef Cattle Research Council, Equine Guelph, and Grayson Jockey Club.

References

Abraham J, Morris D, Griffeth G, Shofer F, Rankin S. 2007. Surveillance of healthy cats and cats with infl ammatory skin disease for colonization of the skin by methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi ssp. schleiferi. Vet Dermatol 18:252-259.

Anderson M, Weese J. 2007. Evaluation of a real-time polymerase chain reaction assay for rapid identifi cation of methicillin-resistant Staphylo-coccus aureus directly from nasal swabs in horses. Vet Microbiol 122:185-189.

Anderson ME, Lefebvre SL, Weese JS. 2008. Evaluation of prevalence and risk factors for methicillin-resistant Staphylococcus aureus colonization in veterinary personnel attending an international equine veterinary conference. Vet Microbiol 129:410-417.

Anderson M, Lefebvre S, Rankin S, Aceto H, Morley P, Caron J, Welsh R, Holbrook T, Moore B, Taylor D, Weese J. 2009. Retrospective multi-centre study of methicillin-resistant Staphylococcus aureus infections in 115 horses. Equine Vet J 41:401-405.

Baptiste K, Williams K, Willams N, Wattret A, Clegg P, Dawson S, Corkill J, O’Neill T, Hart C. 2005. Methicillin-resistant staphylococci in com-panion animals. Emerg Infect Dis 11:1942-1944.

Boost M, O’Donoghue M, Siu K. 2007a. Characterisation of methicillin-resistant Staphylococcus aureus isolates from dogs and their owners. Clin Microbiol Infect 13:731-733.

Boost MV, O’Donoghue MM, James A. 2007b. Prevalence of Staphylococcus aureus carriage among dogs and their owners. Epidemiol Infect:1-12.

Burstiner L, Faires M, Weese JS. 2009. Methicillin-resistant Staphylococ-cus aureus colonization of veterinary personnel at a surgical conference. American Society for Microbiology (ASM)-ESCMID Conference on Methicillin-Resistant Staphylococci in Animals, London.

Burton S, Reid-Smith R, McClure JT, Weese JS. 2008. Staphylococcus aureus colonization in healthy horses in Atlantic Canada. Can Vet J 49:797-799.

Chambers HF, DeLeo FR. 2009. Waves of resistance: Staphylococcus au-reus in the antibiotic era. Nat Rev Microbiol 7:629-641.

Christianson S, Golding G, Campbell J, Canadian Nosocomial Infection Surveillance Program, Mulvey M. 2007. Comparative genomics of Ca-nadian epidemic lineages of methicillin-resistant Staphylococcus au-reus. J Clin Microbiol 45:1904-1911.

Cui S, Li J, Hu C, Jin S, Li F, Guo Y, Ran L, Ma Y. 2009. Isolation and characterization of methicillin-resistant Staphylococcus aureus from swine and workers in China. J Antimicrob Chemother 64:680-683.

Cuny C, Kuemmerle J, Stanek C, Willey B, Strommenger B, Witte W. 2006. Emergence of MRSA infections in horses in a veterinary hospital: Strain characterisation and comparison with MRSA from humans. Euro Sur-veill 11:44-47.

Cuny C, Strommenger B, Witte W, Stanek C. 2008. Clusters of infections in horses with MRSA ST1, ST254, and ST398 in a veterinary hospital. Microb Drug Resist 14:307-310.

de Boer E, Zwartkruis-Nahuis JT, Wit B, Huijsdens X, de Neeling A, Bosch T, van Oosterom RA, Vila A, Heuvelink AE. 2009. Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Micro-biol 134:52-56.

de Neeling A, van den Broek M, Spalburg E, van Santen-Verheuvel M, Dam-Deisz W, Boshuizen H, van de Giessen A, van Duijkeren E, Huijsdens X. 2007. High prevalence of methicillin resistant Staphylo-coccus aureus in pigs. Vet Microbiol 122:366-372.

Denis O, Suetens C, Hallin M, Catry B, Ramboer I, Dispas M, Willems G, Gordts B, Butaye P, Struelens MJ. 2009. Methicillin-resistant Staphylo-coccus aureus ST398 in swine farm personnel, Belgium. Emerging Infect Dis 15:1098-1101.

Devriese LA, Van Damme LR, Famaree L. 1972. Methicillin (cloxacillin)-resistant Staphylococcus aureus strains isolated from bovine mastitis cases. Zentralbl Veterinarmed B 19:598-605.

Dewaele I, De Man I, Stael A, Delputte P, Butaye P, Vlaemynck G, Herman L, Heyndrickx M, Rasschaert G. 2008. Methicillin-resistant Staphylo-coccus aureus (MRSA) in Belgian pig farms. American Society for Mi-crobiology (ASM) Conference on Antimicrobial Resistance in Zoonotic Bacteria and Foodborne Pathogens, Copenhagen.

Diederen B, Kluytmans J. 2006. The emergence of infections with community-associated methicillin resistant Staphylococcus aureus. J Infect 52:157-168.

Enoch D, Karas J, Slater J, Emery M, Kearns A, Farrington M. 2005. MRSA carriage in a pet therapy dog. J Hosp Infect 60:186-188.

Faires MC, Tater KC, Weese JS. 2009. An investigation of methicillin-resistant Staphylococcus aureus colonization in people and pets in the same household with an infected person or infected pet. JAVMA 235:540-543.

Frazee B, Lynn J, Charlebois E, Lambert L, Lowery D, Perdreau-Remington F. 2005a. High prevalence of methicillin-resistant Staphylococcus au-reus in emergency department skin and soft tissue infections. Ann Emerg Med 45:311-320.

Frazee B, Salz T, Lambert L, Perdreau-Remington F. 2005b. Fatal community-associated methicillin-resistant Staphylococcus aureus pneumonia in an immunocompetent young adult. Ann Emerg Med 46:401-404.

Golding GR, Levett PN, McDonald RR, Wylie J, Mulvey MR. 2009. Mo-lecular characterization of the fi rst clinical infections of “livestock as-sociated” ST398 methicillin-resistant Staphylococcus aureus in Canada. American Society for Microbiology (ASM)-ESCMID Conference on Methicillin-Resistant Staphylococci in Animals, London.

Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE, Jensen BJ, Killgore G, Tenover FC, Kuehnert MJ. 2008. Changes in the prevalence of nasal colonization with Staphylococ-cus aureus in the United States, 2001-2004. J Infect Dis 197:1226-1234.

Graveland H, Wagenaar JA, Broekhuizen-Stins MJ, Oosting-Schothorst I, Schoormans AH, van Duijkeren E, Huijsdens X, Mevius D, Heederik D. 2008. Methicillin-resistant Staphylococcus aureus (MRSA) in veal calf farmers and veal calves in the Netherlands. American Society for Mi-crobiology (ASM) Conference on Antimicrobial Resistance in Zoonotic Bacteria and Foodborne Pathogens, Copenhagen. p 62-63.

Griffeth GC, Morris DO, Abraham JL, Shofer FS, Rankin SC. 2008. Screen-ing for skin carriage of methicillin-resistant coagulase-positive staphy-lococci and Staphylococcus schleiferi in dogs with healthy and infl amed skin. Vet Dermatol 19:142-149.

Grinberg A, Kingsbury DD, Gibson IR, Kirby BM, Mack HJ, Morrison D. 2008. Clinically overt infections with methicillin-resistant Staphylococcus aureus in animals in New Zealand: A pilot study. NZ Vet J 56:237-242.

Guardabassi L, Stegger M, Skov R. 2007. Retrospective detection of methi-cillin resistant and susceptible Staphylococcus aureus ST398 in Danish slaughter pigs. Vet Microbiol 122:384-386.

242 ILAR Journal

Hanselman B, Kruth S, Rousseau J, Low D, Willey B, McGeer A, Weese J. 2006. Methicillin-resistant Staphylococcus aureus colonization in vet-erinary personnel. Emerg Infect Dis 12:1933-1938.

Hanselman BA, Kruth S, Weese JS. 2007. Methicillin-resistant staphylo-coccal colonization in dogs entering a veterinary teaching hospital. Vet Microbiol 126:277-281.

Hanselman BA, Kruth SA, Rousseau J, Weese JS. 2008. Methicillin-resistant Staphylococcus aureus colonization in schoolteachers in Ontario. Can J Infect Dis Med Microbiol 19:405-408.

Hanselman BA, Kruth SA, Rousseau J, Weese JS. 2009. Coagulase positive staphylococcal colonization of people and their household pet. Can Vet J 50:954-958.

Harper AL, Male MJ, Scheibel RP, Hanson BM, Wardyn SE, Smith TC. 2009. Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in organic and confi nement swine operations in the midwestern United States. American Society for Microbiology (ASM)-ESCMID Confer-ence on Methicillin-Resistant Staphylococci in Animals, London.

Hartmann FA, Trostle SS, Klohnen AA. 1997. Isolation of methicillin-resis-tant Staphylococcus aureus from a postoperative wound infection in a horse. JAVMA 211:590-592.

Hasman H, Moodley A, Guardabassi L, Stegger M, Skov RL, Aarestrup FM. 2010. Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet Microbiol 141:326-331.

Huber H, Koller S, Giezendanner N, Stephan R, Zeweifel C. 2009. Methi-cillin-resistant Staphylococcus aureus (MRSA) in livestock animals and foods of animal origin in Switzerland. American Society for Microbiol-ogy (ASM)-ESCMID Conference on Methicillin-Resistant Staphylo-cocci in Animals, London.

Huijsdens X, van Dijke B, Spalburg E, van Santen-Verheuvel M, Heck M, Pluister G, Voss A, Wannet W, de Neeling A. 2006. Community-acquired MRSA and pig-farming. Ann Clin Microbiol Antimicrob 5:26.

Jones T, Kellum M, Porter S, Bell M, Schaffner W. 2002. An outbreak of community-acquired foodborne illness caused by methicillin-resistant staphylococcus aureus. Emerg Infect Dis 8:82-84.

Juhász-Kaszanyitzky E, Jánosi S, Somogyi P, Dán A, van der Graaf-van Bloois L, van Duijkeren E, Wagenaar J. 2007. MRSA transmission be-tween cows and humans. Emerg Infect Dis 13:630-632.

Khanna T, Friendship R, Dewey C, Weese JS. 2007. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Micro-biol 128:298-303.

Kluytmans J, van Leeuwen W, Goessens W, Hollis R, Messer S, Herwaldt L, Bruining H, Heck M, Rost J, van Leeuwen N. 1995. Food-initiated outbreak of methicillin-resistant Staphylococcus aureus analyzed by pheno- and genotyping. J Clin Microbiol 33:1121-1128.

Köck R, Harlizius J, Bressan N, Laerberg R, Wieler LH, Witte W, Deurenberg RH, Voss A, Becker K, Friedrich AW. 2009. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Eur J Clin Microbiol Infect Dis 28:1375-1382.

Kottler S, Middleton JR, Weese JS, Cohn L. 2008. Prevalence of Staphylo-coccus aureus and MRSA carriage in three populations. 26th Annual Conference of the American College of Veterinary Internal Medicine, San Antonio.

Kwon NH, Park KT, Moon JS, Jung WK, Kim SH, Kim JM, Hong SK, Koo HC, Joo YS, Park YH. 2005. Staphylococcal cassette chromo-some MEC (SCCMEC) characterization and molecular analysis for methicillin-resistant Staphylococcus aureus and novel SCCMEC sub-type IVG isolated from bovine milk in Korea. J Antimicrob Chemother 56:624-632.

Lee J. 2003. Methicillin (oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl Environ Microbiol 69:6489-6494.

Lee J. 2006. Occurrence of methicillin-resistant Staphylococcus aureus strains from cattle and chicken, and analyses of their mecA, mecR1 and mecI genes. Vet Microbiol 114:155-159.

Lefebvre SL, Weese JS. 2009. Contamination of pet therapy dogs with MRSA and Clostridium diffi cile. J Hosp Infect 72:268-269.

Lefebvre SL, Reid-Smith RJ, Waltner-Toews D, Weese JS. 2009. Inci-dence of acquisition of methicillin-resistant Staphylococcus aureus, clostridium diffi cile, and other health-care-associated pathogens by dogs that participate in animal-assisted interventions. JAVMA 234:1404-1417.

Leonard F, Abbott Y, Rossney A, Quinn P, O’Mahony R, Markey B. 2006. Methicillin-resistant Staphylococcus aureus isolated from a veterinary surgeon and fi ve dogs in one practice. Vet Rec 158:155-159.

Lewis HC, Mølbak K, Reese C, Aarestrup FM, Selchau M, Sørum M, Skov RL. 2008. Pigs as source of methicillin-resistant Staphylococcus aureus cc398 infections in humans, Denmark. Emerging Infect Dis 14:1383-1389.

Lin J, Yeh KS, Liu HT, Lin JH. 2009. Staphylococcus aureus isolated from pork and chicken carcasses in Taiwan: Prevalence and antimicrobial susceptibility. J Food Prot 72:608-611.

Loeffl er A, Boag A, Sung J, Lindsay J, Guardabassi L, Dalsgaard A, Smith H, Stevens K, Lloyd D. 2005. Prevalence of methicillin-resistant Staph-ylococcus aureus among staff and pets in a small animal referral hospi-tal in the UK. J Antimicrob Chemother 56:692-697.

Loeffl er A, Pfeiffer DU, Lindsay JA, Soares-Magalhaes R, Lloyd DH. 2010. Lack of transmission of methicillin-resistant Staphylococcus aureus (MRSA) between apparently healthy dogs in a rescue kennel. Vet Mi-crobiol 141:178-181.

Lozano C, López M, Gómez-Sanz E, Ruiz-Larrea F, Torres C, Zarazaga M. 2009. Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain. J Antimicrob Chemother 64:1325-1326.

Malik S, Coombs G, O’Brien F, Peng H, Barton M. 2006. Molecular typing of methicillin-resistant staphylococci isolated from cats and dogs. J Antimicrob Chemother 58:428-431.

Manian FA. 2003. Asymptomatic nasal carriage of mupirocin-resistant, methicillin-resistant Staphylococcus aureus (MRSA) in a pet dog asso-ciated with MRSA infection in household contacts. Clin Infect Dis 36:e26-e28.

Middleton J, Fales W, Luby C, Oaks J, Sanchez S, Kinyon J, Wu C, Maddox C, Welsh R, Hartmann F. 2005. Surveillance of Staphylococcus aureus in veterinary teaching hospitals. J Clin Microbiol 43:2916-2919.

Miller L, Perdreau-Remington F, Rieg G, Mehdi S, Perlroth J, Bayer A, Tang A, Phung T, Spellberg B. 2005. Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med 352:1445-1453.

Moodley A, Stegger M, Bagcigil A, Baptiste K, Loeffl er A, Lloyd D, Williams N, Leonard N, Abbott Y, Skov R, Guardabassi L. 2006. Spa typing of methicillin-resistant Staphylococcus aureus isolated from do-mestic animals and veterinary staff in the UK and Ireland. J Antimicrob Chemother 58:1118-1123.

Moodley A, Nightingale EC, Stegger M, Nielsen SS, Skov RL, Guardabassi L. 2008. High risk for nasal carriage of methicillin-resistant Staphylo-coccus aureus among Danish veterinary practitioners. Scand J Work Env Health 34:151-157.

Moon JS, Lee AR, Kang HM, Lee ES, Kim MN, Paik YH, Park YH, Joo YS, Koo HC. 2007. Phenotypic and genetic antibiogram of methicillin-resistant staphylococci isolated from bovine mastitis in Korea. J Dairy Sci 90:1176-1185.

Morris D, Mauldin E, O’Shea K, Shofer F, Rankin S. 2006a. Clinical, microbiological, and molecular characterization of methicillin-resis-tant Staphylococcus aureus infections of cats. Am J Vet Res 67:1421-1425.

Morris D, Rook K, Shofer F, Rankin S. 2006b. Screening of Staphylococcus aureus, Staphylococcus intermedius, and Staphylococcus schleiferi iso-lates obtained from small companion animals for antimicrobial resis-tance: A retrospective review of 749 isolates (2003-04). Vet Dermatol 17:332-337.

Nemati M, Hermans K, Lipinska U, Denis O, Deplano A, Struelens M, Devriese LA, Pasmans F, Haesebrouck F. 2008. Antimicrobial resis-tance of old and recent Staphylococcus aureus isolates from poultry: First detection of livestock-associated methicillin-resistant strain ST398. Antimicrob Agents Chemother 52:3817-3819.

Volume 51, Number 3 2010 243

Nienhoff U, Kadlec K, Chaberny IF, Verspohl J, Gerlach GF, Schwarz S, Simon D, Nolte I. 2009. Transmission of methicillin-resistant Staphylo-coccus aureus strains between humans and dogs: Two case reports. J Antimicrob Chemother 64:660-662.

O’Mahony R, Abbott Y, Leonard F, Markey B, Quinn P, Pollock P, Fanning S, Rossney A. 2005. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from animals and veterinary personnel in ireland. Vet Microbiol 109:285-296.

Persoons D, Van Hoorebeke S, Hermans K, Butaye P, de Kruif A, Haesebrouck F, Dewulf J. 2009. Methicillin-resistant Staphylococcus aureus in poul-try. Emerging Infect Dis 15:452-453.

Pu S, Han F, Ge B. 2009. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Envi-ron Microbiol 75:265-267.

Rivas K, Garcia A, Morales PR, Matchett CA, Saucedo A, Wagner JL. 2007. Methicillin-resistant Staphylococcus aureus (MRSA) pneumonia in a rhesus macaque [abstract]. JAALAS 46:102.

Schwarz S, Kadlec K, Strommenger B. 2007. Methicillin-resistant Staphy-lococcus aureus and staphylococcus pseudintermedius detected in the BFT-germvet monitoring programme 2004-2006 in Germany. J Antimi-crob Chemother 61:282-285.

Seguin JC, Walker RD, Caron JP, Kloos WE, George CG, Hollis RJ, Jones RN, Pfaller MA. 1999. Methicillin-resistant Staphylococcus aureus out-break in a veterinary teaching hospital: Potential human-to-animal transmission. J Clin Microbiol 37:1459-1463.

Sergio D, Koh T, Hsu L, Ogden B, Goh A, Chow P. 2007. Investigation of methicillin-resistant Staphylococcus aureus in pigs used for research. J Med Microbiol 56:1107-1109.

Shimizu A, Kawano J, Yamamoto C, Kakutani O, Anzai T, Kamada M. 1997. Genetic analysis of equine methicillin-resistant Staphylococcus aureus by pulsed-fi eld gel electrophoresis. J Vet Med Sci 59:935-937.

Sing A, Tuschak C, Hörmansdorfer S. 2008. Methicillin-resistant Staphylo-coccus aureus in a family and its pet cat. N Engl J Med 358:1200-1201.

Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP, Moritz ED, Capuano AW, Herwaldt LA, Diekema DJ. 2008a. Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in Midwestern US swine and swine workers. PLoS ONE 4:e4258.

Smith TC, Male MJ, Harper AL, Moritz-Korolev E, Kroeger JS, Diekema DJ, Herwaldt LA. 2008b. Isolation of methicillin-resistant Staphylococ-cus aureus (MRSA) from swine in the midwestern United States. Inter-national Conference on Emerging Infectious Diseases, Atlanta.

Strommenger B, Kehrenberg C, Kettlitz C, Cuny C, Verspohl J, Witte W, Schwarz S. 2006. Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates. J Antimicrob Chemother 57:461-465.

Taylor WM, Grady AW. 1998. Catheter-tract infections in rhesus macaques (Macaca mulatta) with indwelling intravenous catheters. Lab Anim Sci 48:448-454.

Tenover FC, McAllister S, Fosheim G, McDougal LK, Carey RB, Limbago B, Lonsway D, Patel JB, Kuehnert MJ, Gorwitz R. 2008. Characteriza-tion of Staphylococcus aureus isolates from nasal cultures collected from individuals in the United States in 2001 to 2004. J Clin Microbiol 46:2837-2841.

Tokateloff, N, Manning ST, Weese JS, Campbell J, Rothenburger J, Stephen C, Bastura V, Gow SP, Reid-Smith R. 2009. Prevalence of methicillin-resistant Staphylococcus aureus colonization in horses in Saskatchewan, Alberta, and British Columbia. Can Vet J 50:1177-1180.

Tomlin J, Pead M, Lloyd D, Howell S, Hartmann F, Jackson H, Muir P. 1999. Methicillin-resistant Staphylococcus aureus infections in 11 dogs. Vet Rec 144:60-64.

van den Broek IV, van Cleef BA, Haenen A, Broens EM, van der Wolf PJ, van den Broek MJ, Huijsdens X, Kluytmans J, van de Giessen AW, Tiemersma E. 2008. Methicillin-resistant Staphylococcus aureus in people living and working in pig farms. Epidemiol Infect:1-9.

Van den Eede A, Martens A, Lipinska U, Struelens M, Deplano A, Denis O, Haesebrouck F, Gasthuys F, Hermans K. 2009. High occurrence of methicillin-resistant Staphylococcus aureus ST398 in equine nasal samples. Vet Microbiol 133:138-144.

van Duijkeren E, Wolfhagen MJ, Heck ME, Wannet WJ. 2005. Transmis-sion of a panton-valentine leucocidin-positive, methicillin-resistant Staphylococcus aureus strain between humans and a dog. J Clin Micro-biol 43:6209-6211.

van Duijkeren E, Jansen MD, Flemming SC, de Neeling H, Wagenaar JA, Schoormans AH, van Nes A, Fluit AC. 2007. Methicillin-resistant Staphy-lococcus aureus in pigs with exudative epidermitis. Emerging Infect Dis 13:1408-1410.

van Duijkeren E, Ikawaty R, Broekhuizen-Stins M, Jansen M, Spalburg E, de Neeling A, Allaart J, van Nes A, Wagenaar J, Fluit A. 2008. Trans-mission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Vet Microbiol 126:383-389.

van Duijkeren E, Moleman M, Sloet van Oldruitenborgh-Oosterbaan MM, Multem J, Troelstra A, Fluit AC, van Wamel WJ, Houwers DJ, de Neel-ing A, Wagenaar JA. 2010. Methicillin-resistant Staphylococcus aureus in horses and horse personnel: An investigation of several outbreaks. Vet Microbiol 141:96-102.

van Loo I, Huijsdens XW, Tiemersma E, de Neeling AJ, van de Sande-Bruinsma N, Beaujean D, Voss A, Kluytmans J. 2007a. Emergence of methicillin-resistant Staphylococcus aureus of animal origin. Emerging Infect Dis 13:1834-1839.

van Loo IH, Diederen BM, Savelkoul PH, Woudenberg JH, Roosendaal R, van Belkum A, Lemmens-den Toom N, Verhulst C, van Keulen PH, Kluytmans JA. 2007b. Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerging Infect Dis 13:1753-1755.

van Rijen MM, Van Keulen PH, Kluytmans JA. 2008. Increase in a Dutch hospital of methicillin-resistant Staphylococcus aureus related to ani-mal farming. Clin Infect Dis 46:261-263.

van Rijen MM, Bosch T, Heck ME, Kluytmans JA. 2009. Methicillin-resistant Staphylococcus aureus epidemiology and transmission in a Dutch hospital. J Hosp Infect 72:299-306.

Vandenbroucke-Grauls CM, Beaujean DJ. 2006. [Methicillin-resistant Staphylococcus aureus in pig breeders and cattle breeders]. Nederlands tijdschrift voor geneeskunde 150:1710-1712.

Vengust M, Anderson M, Rousseau J, Weese J. 2006. Methicillin-resistant staphylococcal colonization in clinically normal dogs and horses in the community. Lett Appl Microbiol 43:602-606.

Vitale C, Gross T, Weese J. 2006. Methicillin-resistant Staphylococcus aureus in cat and owner. Emerging Infect Dis 12:1998-2000.

Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M. 2005. Methicillin-resistant Staphylococcus aureus in pig farming. Emerging Infect Dis 11:1965-1966.

Wagenaar JA, Yue H, Pritchard J, Broekhuizen-Stins M, Huijsdens X, Mevius DJ, Bosch T, van Duijkeren E. 2009. Unexpected sequence types in livestock associated methicillin-resistant Staphylococcus au-reus (MRSA): MRSA ST9 and a single locus variant of ST9 in pig farm-ing in China. Vet Microbiol 139:405-409.

Walther B, Monecke S, Ruscher C, Friedrich AW, Ehricht R, Slickers P, Soba A, Wleklinski CG, Wieler LH, Lübke-Becker A. 2009. Comparative molecular analysis substantiates zoonotic potential of equine methicillin-resistant Staphylococcus aureus. J Clin Microbiol 47:704-710.

Weese JS, Lefebvre SL. 2007. Risk factors for methicillin-resistant Staphy-lococcus aureus colonization in horses admitted to a veterinary teaching hospital. Can Vet J 48:921-926.

Weese J, Rousseau J. 2005. Attempted eradication of methicillin-resistant Staphylococcus aureus colonisation in horses on two farms. Equine Vet J 37:510-514.

Weese J, Archambault M, Willey B, Hearn P, Kreiswirth B, Said-Salim B, McGeer A, Likhoshvay Y, Prescott J, Low D. 2005a. Methicillin-resistant Staphylococcus aureus in horses and horse personnel, 2000-2002. Emerging Infect Dis 11:430-435.

Weese J, Rousseau J, Traub-Dargatz J, Willey B, McGeer A, Low D. 2005b. Community-associated methicillin-resistant Staphylococcus aureus in horses and humans who work with horses. JAVMA 226:580-583.

Weese J, Caldwell F, Willey B, Kreiswirth B, McGeer A, Rousseau J, Low D. 2006a. An outbreak of methicillin-resistant Staphylococcus aureus skin infections resulting from horse to human transmission in a veteri-nary hospital. Vet Microbiol 114:160-164.

244 ILAR Journal

Weese J, Dick H, Willey B, McGeer A, Kreiswirth B, Innis B, Low D. 2006b. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet Microbiol 115:148-155.

Weese J, Rousseau J, Willey B, Archambault M, McGeer A, Low D. 2006c. Methicillin-resistant Staphylococcus aureus in horses at a veterinary teaching hospital: Frequency, characterization, and association with clinical disease. J Vet Intern Med 20:182-186.

Weese JS, Faires M, Rousseau J, Bersenas AM, Mathews KA. 2007. Cluster of methicillin-resistant Staphylococcus aureus colonization in a small animal intensive care unit. JAVMA 231:1361-1364.

Weese JS, Avery B, Rousseau J, Reid-Smith R. 2009a. Methicillin-resistant Staphylococcus aureus contamination of retail meat: Canada. American Society for Microbiology (ASM)-ESCMID Conference on Methicillin-Resistant Staphylococci in Animals, London.

Weese JS, Avery BP, Gow S, Booker C, Reid-Smith R. 2009b. Methicillin- resistant Staphylococcus aureus (MRSA) surveillance in slaughter-age pigs and feedlot cattle. American Society for Microbiology (ASM)-ESCMID Conference on Methicillin-Resistant Staphylococci in Animals, London.

Weese JS, Friendship R, Wakeford T, Zwambag A, Rousseau J, Reid-Smith R. 2009c. Longitudinal evaluation of methicillin-resistant

Staphylococcus aureus and Clostridium diffi cile in pigs. European Conference of Clinical Microbiology and Infectious Diseases, Hel-sinki.

Witte W, Strommenger B, Stanek C, Cuny C. 2007. Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, central Europe. Emerging Infect Dis 13:255-258.

Wulf M, van Nes A, Eikelenboom-Boskamp A, de Vries J, Melchers W, Klaassen C, Voss A. 2006. Methicillin-resistant Staphylococcus aureus in veterinary doctors and students, the Netherlands. Emerging Infect Dis 12:1939-1941.

Wulf MW, Sørum M, van Nes A, Skov R, Melchers WJ, Klaassen CH, Voss A. 2007. Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: An international study. Clin Microbiol Infect 14:519-521.

Wulf MW, Tiemersma E, Kluytmans J, Bogaers D, Leenders AC, Jansen MW, Berkhout J, Ruijters E, Haverkate D, Isken M, Voss A. 2008. MRSA carriage in healthcare personnel in contact with farm animals. J Hosp Infect 70:186-190.

Zemlicková H, Fridrichová M, Tyllová K, Jakubů V, Machová I. 2009. Carriage of methicillin-resistant Staphylococcus aureus in veterinary personnel. Epidemiol Infect 137:1233-1236.