Antimicrobial use

Backgrounders

Policy

Reports

Miscellaneous

= AVMA/SAVMA  Members Only

Some files on this page require Adobe Reader software. Click on the image above to download it for free from the Adobe site.

FAQs for animal owners

Information for human healthcare providers

Causative agent
Methicillin-resistant Staphylococcus aureus (MRSA) is a Gram-positive bacterium that is resistant to methicillin (a member of the penicillin family) and many other β-lactam antimicrobials; β-lactam antimicrobials include penicillins and cephalosporins. The description "Methicillin-resistant" was first used in 1961, based on the discovery of a Staphyloccocus aureus infection in the United Kingdom that was resistant to methicillin.¹ Since that time, MRSA has emerged as a significant problem worldwide, and the term has evolved to include resistance to additional β-lactam antimicrobials. Currently, the term MRSA is often used to describe multi-drug resistant Staphylococcus aureus.

Resistance is mediated by a gene (mecA) that encodes the production of an altered penicillin-binding protein (PBP2a), which does not allow for the binding of β-lactams to the bacterial cell wall.² Because β-lactams exert antibacterial activity by binding and inhibiting enzymes necessary for bacterial cell wall synthesis, these antimicrobials are not effective against MRSA.

Background
Staphylococcus aureus (S. aureus) is a major pathogen in both nosocomial (hospital-acquired) and community-acquired infections worldwide, and according to the Centers for Disease Control and Prevention (CDC), is one of the most common causes of human skin and soft tissue infections in the United States. Clinical signs range from minor skin conditions (e.g., pimples, boils and impetigo) to more severe disease such as cellulitis and postoperative wound infections. S. aureus can also cause pneumonia, bacteremia, meningitis, sepsis, and pericarditis.³
S. aureus bacteria are commonly carried on the skin or in the nasal passages of healthy people and animals. A person (or animal) that carries the bacteria on their body but does not exhibit signs of disease is considered to be "colonized". Approximately 25 to 40% of the human population is colonized by S. aureus, mainly in the nasal passages. Although primary MRSA infections in immunocompetent people are quite common, immunocompromised individuals are more likely to develop infection. S. aureus also tends to cause infections in people who are in compromised environments such as hospitals, chronic care facilities, prisons, housing projects, or in other crowded settings, such as schools and public events. ^4-7

Penicillin was originally found to be extremely effective in treating S. aureus infections, but penicillin-resistant strains of S. aureus, mediated by the production of β-lactamase (an enzyme that inactivates the lactam ring of β-lactam antibiotics), began to develop. Methicillin was introduced in 1959 to treat human patients with staphylococcal infections resistant to penicillin. Although methicillin is relatively resistant to β-lactamase, MRSA isolates were reported in Great Britain in 1961.⁸ By the mid-1970s MRSA had become endemic in many countries.^2,9 Further, in addition to being resistant to β-lactam antimicrobials, many MRSA strains are resistant to various other antimicrobial classes, and treatment options may be limited in many cases.

MRSA Terminology
Community-Associated and Hospital-Associated MRSA
Community-associated MRSA (CA-MRSA) infections occur in otherwise healthy people without a recent history of hospitalization or medical procedures, and are usually associated with skin and soft tissue infection. Risk factors for CA-MRSA include crowding, frequent contact, compromised skin, contaminated surfaces and shared items, and poor hygiene.¹⁰

Nosocomial, or hospital-associated MRSA (HA-MRSA)
Hospital-associated MRSA (HA-MRSA)infections occur most commonly in immunocompromised individuals in hospitals and healthcare centers. Risk factors for HA-MRSA include hospitalization, surgery, dialysis, long-term care, indwelling devices, and history of previous MRSA infection. To date, the majority of clinically significant MRSA infections are HA-MRSA.^11,12
MRSA Typing and Nomenclature

MRSA nomenclature varies worldwide, and a standard method for typing and naming MRSA strains has not yet been adopted. MRSA strains can be typed by both phenotypic and molecular methods. Phenotypic methods include: colonial characteristics, biochemical reactions, antibiotic susceptibility pattern, and the susceptibility to various phages and toxin production. The most prominent molecular typing methods are: pulsed field gel electrophoresis (PFGE), multilocus sequence typing(MLST), SCCmec and spa typing. There is a new typing method that uses several variable number tandem repeat (VNTR) sequences for typing of animal MRSA isolates, but to date there is no published data available. ¹³

Infection with the MRSA strain USA100 (CA-MRSA-2, ST5-MRSA-SCCmecII) has been shown to be more predominant in small animals, while infection with the MRSA strain USA500 (CMRSA-5, ST8-MRSA SCCmecIV) has been shown to be more predominant in large animals.¹² To date, the data are still emerging and are subject to change.

Transmission
For many years, MRSA was considered only a human pathogen, until a report of a MRSA infection in a dairy cow surfaced in 1972.¹⁴ It has now become an increasingly urgent problem in veterinary medicine, with MRSA infections reported in horses, dogs, cats, pet birds, cattle and pigs.^2,12,15-23 CA-MRSA in humans is thought to be a major factor in the rise of MRSA infection in animals such as dogs, cats, pet birds, and horses.^2,12,18,23 The predominant strain in food animals (eg, pigs, cattle) seems to be animal in origin and it's emergence is probably unrelated to the epidemiology of MRSA in the community. It was first thought that the transmission of MRSA transmission was solely from human to animal, with MRSA colonization and infection typically occurring with contact between the hands of the human and anterior nares (nostrils) of the animal. There is now increasing evidence that MRSA can be transmitted in both directions, from human to animal and from animal to human. Once exposed to MRSA, animals can become colonized, and may serve as reservoirs to transmit the infection to other animals and also to their human handlers.^{2,12,18,23,24} This has been documented in both the general community and in animal nosocomial environments (eg, veterinary clinics and hospitals, farms, and slaughterhouses).^20,24-26 Data have indicated that owners and veterinary personnel that come into contact with MRSA-infected animals may become colonized by MRSA. There is then a risk that subsequent contact with susceptible animals or human beings will transfer MRSA infection.^2,27 With human-to-animal transmission of MRSA, there is a possibility that until the animal is free of infection, re-transmission from animal to human and subsequent human-to-human transmission can occur.^15,18,24 In one reported case of possible dog-to-human transmission, a diabetes mellitus patient and his wife experienced recurrent MRSA infections and difficulty in eliminating MRSA (decolonization). A nares culture of the family dog revealed it was colonized with MRSA, and long-term decolonization for the man and his wife occurred only after the dog was treated.²⁴ However, there was no clear evidence that the dog was the source of infection. There is a concern that antimicrobial treatment of MRSA in companion animals may increase antimicrobial resistance, and have a subsequent effect on the zoonotic transmission or re-transmission to humans, especially if the humans involved are already in an immunocompromised state.¹⁸

Zoonotic transmission of MRSA should be considered an occupational risk for veterinary professionals, especially those in large animal practices.¹² It has been shown that even apparently healthy animals may be MRSA reservoirs, and therefore may pose a risk to their handlers.^16,23 Ongoing MRSA surveillance in animals for both colonization and infection is necessary in order to clarify the epidemiology of the transmitted strains as well as develop measures to reduce transmission.¹⁹

Few data on MRSA colonization rates in non-clinically affected animals are available. Although identification of colonized or infected animals is important in the prevention of the spread of MRSA, the routine screening of all animals is not yet practical, so there remains the possibility that a small percentage of colonized animals will remain undetected upon first admission to a veterinary clinic.¹³

In a survey by Weese et al, the reported colonization incidence rate of MRSA in horses admitted to a veterinary teaching hospital was 27/1000 admissions.²⁸ In a survey conducted in Ireland by Abbott et al, a 0.6% prevalence of MRSA colonization was detected in non-clinically infected dogs upon admission to veterinary clinics, and a 0.9% prevalence of MRSA colonization was detected upon admission of non-clinically infected dogs to a veterinary referral hospital.²⁹

Farmers are at risk of being MRSA reservoirs. In a survey by Voss et al of pig farrners in the Netherlands, 23% (6/26) of pig farmers were colonized with MRSA, a rate that was 760 times higher than the general Dutch population.³⁰ Huijsdens et al noted that the MRSA strains isolated from pig farmers were similar to those seen in pigs.²³

Veterinary personnel are also at risk of being MRSA reservoirs. At the 2005 American College of Veterinary Internal Medicine (ACVIM) Forum, 6.5% of the attending veterinary personnel who volunteered to be tested were found to be colonized with MRSA. In this study, the volunteers provided a nasal swab and completed a questionnaire that identified potential risk factors for MRSA colonization. None of those who tested positive had a recent history of hospitalization or previous diagnosis of MRSA. Large animal practice was the only significant risk factor for MRSA colonization, with 12/271 (4.4%) small animal practice personnel colonized, and 15/96 (15.6%) of large animal practice personnel colonized (P < 0.001). A significant difference was found between the MRSA clones found in veterinary personnel from large animal practices (the USA500/CMRSA-5 strain) compared to the MRSA clones found in veterinary personnel from small animal practices (the USA100/CMRSA-2 strain).³¹

There has been considerable controversy regarding the link between antimicrobial use in livestock and MRSA. In a Netherlands study, the predominant antimicrobials used in livestock were tetracycline and trimethoprim/sulfonamide combinations, and all the MRSA strains in the study were found to be resistant to tetracycline.²² Further studies are needed to determine the exact sources of MRSA in animals, and the impact of the use of antimicrobial agents in livestock.

The possibility that there may be a transmission route of MRSA from animals to humans via animal food products requires further investigation to determine its public health significance.^17,32Preliminary data in abstracts indicate an MRSA prevalence of 5 to 15% in foods originating from animals. To date, there have been no confirmed cases of food from an infected animal causing an MRSA infection in humans.¹⁷ Reported food-borne MRSA outbreaks have occurred through contamination by infected food handlers. These outbreaks can be minimized by proper food handling and pasteurization.^33,34

Clinical Signs
Not all animals who encounter MRSA develop clinical signs. While research is ongoing, it appears that only a small percentage become ill, while most eliminate the organism or become colonized without developing clinical signs. Among animals, the most commonly reported clinical signs are postoperative and wound infections, with less-reported incidences of intravenous catheter site infections, urinary tract infections, pneumonia, skin, and ear infections, with skin and ear infections the most common.^2,19 CA-MRSA strains that cause skin and soft tissue infections (SSTIs) sometimes contain Panton-Valentin leukocidin exotoxin (PVL) It is unclear whether PVL is a relevant virulence factor or a marker for some other factor, a toxin that produces tissue necrosis (tissue death). CA-MRSA infection may present as a red, swollen, painful site with drainage.³

Diagnosis
Proper MRSA diagnosis may be a potential problem since samples are sent to different diagnostic laboratories that may not be uniform in the testing of the bacterial species and their antibiotic sensitivities. Diagnosis should involve the identification of coagulase-positive Staphylococci to the species level, and all S. aureus isolates should then be tested for oxacillin resistance, since methicillin is less stable in vitro. Veterinary laboratories that are not familiar with oxacillin-resistant S. aureus should make sure that their routine screens for oxacillin resistance are supplemented with multiple tests to confirm the presence of PBP2a (mecA) in isolates that exhibit borderline susceptibility.³⁵

If there is a recurrent or persistent case of skin infection in the animal, a small biopsy of either the infected skin or a sample of the exudate (drainage) from the site may be submitted for laboratory diagnosis. A sputum culture is recommended for pneumonia; and blood or urine cultures are recommended for bloodstream and urinary infections, respectively. If S.aureus is isolated, further tests are needed to determine if it is an MRSA strain, and which antibiotics would be effective for therapy.³.

Rapid diagnosis of MRSA in animals is still in its early stages of development, and to date there is still a significant delay between sample collection and obtaining test results for animals, as compared to humans.² Rapid tests that have been validated for use in humans (i.e. real time PCR) do not necessarily perform adequately in animals,so species-specific validation is required.³⁶

Treatment
Despite the increase in reported cases of MRSA in animals, there has been minimal research into the risk factors involved and what treatment regimens are needed in MRSA-infected animals.² When animals are found (usually through swabs of the anterior nares, or nostrils) to be colonized with MRSA, there is currently no recognized method of decolonizing these animals. Based on clinical cases observed, some experts have indicated that companion animals are generally transient carriers of MRSA, so decolonization is either unnecessary or the treatment could be as simple as isolation from the individual who keeps transferring the MRSA back to the pet.³⁷ In cases of skin infections, which are the most common manifestations of MRSA in animals, it has been suggested that a combination of systemic therapy with topical antimicrobial treatment of mucosal sites may have some effect.²⁷ However, van Duijkeren et al have suggested that while systemic therapy is needed, topical treatment with antimicrobials may be impractical based on cost and the difficulty in adequate application of topical ointment into the nasal passages. It has been speculated that both these treatments may lead to further microbial resistance.^38,39 If antibiotic treatment is necessary, it should be guided by the susceptibility profile of the organism.³ However, there are alternative methods that may be used in place of or in combination with antimicrobial therapy. Leonard et al suggested that in the case of patients with imbedded devices (eg, catheters), the removal of the device may be a proper step removing the source of MRSA infection.¹³ Weese et al suggested that the decolonization of horses with MRSA may be accomplished without the use of antimicrobial therapy by using segregation and repeated screening.²⁰

Morbidity and Mortality
In the United States, MRSA is the 10^th leading cause of death in humans, and is the most frequently identified antimicrobial drug-resistant pathogen in hospitals and other healthcare facilities.⁴⁰ In a 2007 report, Klevens et all reviewed the 8987 observed cases of invasive MRSA reported to the Active Bacterial Core surveillance (ABCs)/Emerging Infections Program Network from July 2004 through December 2005. Most (58.4%) of the MRSA infections were health care-associated: 6484 (72.1%) were CA-MRSA infections, 2389 (26.6%) were HA-MRSA infections, and 114 (1.3%) could not be classified. In 2005, the standardized incidence rate of invasive MRSA was 31.8 per 100,000 (interval estimate, 24.4-35.2).¹¹ The increasing prevalence of MRSA in humans is in part a result of the infection emerging from a mainly HA-MRSA source into a CA-MRSA source over the last 10 years.^2,40

Morbidity and mortality data in animals are lacking, and further study is necessary. Morris et al reported that MRSA appeared only as a secondary infection in domestic cats who had predisposing diseases, which suggests that, like humans, MRSA infections are more common in immunocompromised animals.²¹ MRSA is emerging in animal species, and should be closely monitored. The major threat of MRSA for animals and their handlers appears to be in zoonotic and interspecies transmission, with the resultant threat of infections that range from skin infections to pneumonia, and in immunocompromised humans, death. There is currently no evidence that MRSA infections in animals have a poorer prognosis than methicillin-susceptible infections if appropriate treatment is provided.^3,18

Prevention and Control
In humans, MRSA rates worldwide have shown a dramatic increase since the end of the last century. In the United States, MRSA prevalence among all hospital S. aureus isolates increased from 2.4% in 1975 to 29% in 1991.⁴¹ Between 1992 and 2003, the proportion of S. aureus isolates from patients in intensive care units that were meticillin-resistant rose from 35.9% to 64.4%.⁴² In England and Wales, the proportion of S. aureus bacteremia due to MRSA increased from 1% to 2% in 1990–1992 to approximately 40% in 2000.⁴³

Caution is advised when extrapolating the guidelines for MRSA control in people to animals because there may be significant differences in the epidemiology of the disease.³¹ At present no controlled studies have been conducted to provide data on key issues such as prevalence and persistence of colonization and infection in animals, the ease of transmission between animals and humans, and the efficacy of decolonization procedures in animals.¹³

When an animal presents with suspect MRSA indications, such as non-healing wounds, non-antibiotic responsive infections, nosocomial infections, as well as animals from a known MRSA-positive environment or who come into contact with healthcare workers should be screened for MRSA.¹³ Animals identified as, or suspected to be, positive should be admitted directly into a consultation room to prevent contact with other animals. The consulting room must then be cleaned and disinfected before another patient is admitted. Upon entry into a veterinary hospital, a known or suspected MRSA-infected animal should be isolated and nursed using barrier nursing precautions.¹³

In a survey conducted by Hanselman et al of veterinary personnel attending the annual American College of Veterinary Internal Medicine Forum held in Baltimore, Maryland, USA, June 3–5, 2005, nasal swabs were provided by 417 attendees from 19 countries. CMRSA-5 (ST8-MRSA-IV, similar to USA500 was isolated from 13 (48%) of 27 colonized persons, all of whom were in large-animal practice. CMRSA-2 (ST5-MRSA-II, similar to USA100) was isolated from 13 (48%) of 27 colonized persons: 11 in small-animal practice and 2 in large-animal practice.¹²

In large animal practices, veterinary personnel routinely wear coveralls and boots as protective clothing. However, MRSA colonization and transmission usually occurs through contact from the hands of the human to the anterior nares (nostrils) of the animal, so masks and gloves should be considered as additional protective measures.²² Anderson et al reported a significant protective effect of hand hygiene in equine veterinarians.⁴⁴

In a Netherlands study by Wulf et al, the overall MRSA prevalence in veterinary doctors and students in large animal practice that had checked into a human hospital was 160 times higher than other patients; which indicates that animal handlers, including veterinary personnel, farmers, and their families should be screened upon checking into a hospital.²²

In order to stop the transmission and re-transmission between humans and their companion animals, efforts need to be made to decontaminate their shared surroundings.¹³ Factors involved in MRSA transmission are: crowding, compromised skin, contaminated items or surfaces, and poor hygiene.⁴This is an area that needs to be addressed in both the human and the veterinary fields.³⁹

In veterinary hospitals, the use of a chlorhexidine surgical scrub has been proven effective in eradicating transmission of S. aureus. Surgical scrubs containing both chlorhexidine and alcohol have been more effective against multiple strains of MRSA.(Kampf, 1998). In a Japanese study, seven disinfectants for hand scrubs and soaks were evaluated against multiple MRSA strains: glutaraldehyde, povidone iodine, and ethanol proved effective. However sodium hypochlorite, benzalkonium chloride, alkyldiaminoethylglycine hydrochloride, and chlorhexidine digluconate were not effective against all strains using the prescribed concentration conditions and exposure time.⁴⁵

In 2005 The American Veterinary Association (AVMA), in partnership with the CDC, conducted an anonymous survey via a questionnaire sent to veterinarians who were randomly selected from the AVMA membership. The survey group was comprised of US small animal, large animal, and equine veterinarians; was conducted to assess both precaution awareness (PA) and veterinarians' perceptions of zoonotic disease risks. Results indicated that, in general, the respondents did not engage in protective behaviors or use personal protective equipment considered appropriate to protect against zoonotic disease transmission. Small animal and equine veterinarians employed in practices that had no written infection control policy were significantly more likely to have low PA ranking. Male gender was associated with low PA ranking among small animal and large animal veterinarians; equine practitioners not working in a teaching or referral hospital were more likely to have lower PA ranking than equine practitioners working in such institutions.⁴⁶

Veterinarians should be aware of the concerns regarding MRSA and should develop an understanding of appropriate disease surveillance, diagnostic testing, and infection control in order to lessen the impact of MRSA on both animals and their caretakers.^2,12,20,30 Veterinarians not only need to practice proper hygiene and prevention of transmission of zoonotic disease in their work environments, they also have a duty to educate the owners/handlers of MRSA-colonized or -infected animals on the risks and proper hygiene prevention when dealing with these animals.

As in human medicine, hand hygiene is an integral part of the prevention of the spread of MRSA between animals and between animals and humans. Frequent hand washing and proper disinfection of hard surfaces and equipment between patients is essential. Alcohol gel pouches should be provided in all consulting rooms, kennels and with uniforms help to remind staff of the need for frequent hand sanitization. Uniforms, including gloves, disposable aprons and masks should be worn when changing dressings on infected wounds or to prevent potential contact with body fluids or contaminated tissues. Eye protection may be worn if splashing or aerosols are expected. All surroundings in the clinic should be kept to a high standard of cleanliness. Although the cleanliness of floors does not appear to be as important as hand-touch sites in the control of human MRSA infections, the situation may be different in veterinary medicine.¹³

With the rise of MRSA as a zoonotic disease in both human-to-animal and animal-to-human transmission, both human healthcare and veterinary care providers are advised to review the infection control guidelines for the prevention and control of MRSA infections in both animals and humans at: http://www.cdc.gov/ncidod/dhqp/ar_mrsa.html, and http://www.avma.org/avmacollections/zu/javma_232_12_1863.pdf (PDF)

It is incumbent upon both the veterinary and human medical professions to improve communication regarding the roles of both animals and humans in MRSA infection. The pressing need for both prudent antimicrobial use and a good general infection control program in human and veterinary healthcare cannot be overstated. The prudent use of antimicrobials in both animals and humans is essential in order to prevent the spread of MRSA strains that are increasingly resistant to known antimicrobials.

This backgrounder was developed in cooperation with the American College of Veterinary Internal Medicine (ACVIM)

Links to More Scientific Information About MRSA

AVMA
http://www.avma.org/services/Compendium_of_Veterinary_Standard_Precautions_2006.pdf (PDF, 2 Mb)
http://www.avma.org/services/model_infection_control_plan.rtf (.rtf)

CDC MRSA
http://www.cdc.gov/ncidod/dhqp/ar_mrsa_ca_clinicians.html#1
http://www.cdc.gov/ncidod/dhqp/ar_MRSA.html
http://www.cdc.gov/ncidod/dhqp/ar_mrsa_in_schools.html
http://www.cdc.gov/ncidod/dhqp/ar_MRSA_ca_public.html

USDA MRSA
http://www.aphis.usda.gov/vs/ceah/cei/taf/emergingdiseasenotice_files/mrsa_122007.pdf (PDF, 131 Kb)

Science and Development Network MRSA
http://www.scidev.net/en/health/antibiotic-resistance/features/antibiotic-resistance-frequently-asked-questions.html

pets-mrsa.com
http://tahilla.typepad.com/petsmrsa/academic_articles/

References

1. Barber M. Methicillin-resistant staphylococci. J Clin Pathol 1961;14:385-393.
2. Weese JS. Methicillin-resistant Staphylococcus aureus:an emerging pathogen in small animals. J Am Anim Hosp Assoc 2005;41:150-157.
3. Community-Associated MRSA Information for Clinicians. Available at: http://www.cdc.gov/ncidod/dhqp/ar_mrsa_ca_clinicians.html#1. Accessed September 16, 2008.
4. Healthcare-Associated Methicillin Resistant Staphylococcus aureus (HA-MRSA). Available at: http://www.cdc.gov/ncidod/dhqp/ar_MRSA.html. Accessed September 16, 2008.
5. Methicillin-Resistant Staphylococcus aureus (MRSA) in Schools. Available at: http://www.cdc.gov/ncidod/dhqp/ar_mrsa_in_schools.html. Accessed September 16, 2008.
6. Community-Associated MRSA Information for the Public. Available at: http://www.cdc.gov/ncidod/dhqp/ar_MRSA_ca_public.html. Accessed September 16th, 2008.
7. MRSA in Healthcare Settings. Available at: http://www.cdc.gov/ncidod/dhqp/ar_MRSA_spotlight_2006.html. Accessed September 16th, 2008.
8. Jevon MP. 'Celbenin' – resistant staphylococci. BMJ.1961;i:124-5.
9. Voss A, Doebbeling BN. 1995. The worldwide prevalence of methicillin-resistant Staphylococcus aureus. .Int J Antimicrob Agents 1995;5:101-106.
10. Naimi TS, LeDell KH, Como-Sabetti K, et al. Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. J Am Med Assoc 2003;290:2976-2984.
11. Klevens RM, Morrison MA, Nadle J. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. J Am Med Assoc 2007; 298:1763-1771.
12. Hanselman BA, Kruth SA, Rousseau J, et al. Methicillin-resistant Staphylococcus aureus colonization in veterinary personnel. Emerg Infect Dis 2006; 12:1933-1938.
13. Leonard FC, Markey BK. Meticillin-resistant Staphylococcus aureus in animals:A review. Veterinar J 2008;175:27-36.
14. Devriese LA, Van Damme LR, Fameree L. Methicillin (cloxacillin)-resistant Staphylococcus aureus strains isolated from bovine mastitis cases. Zbl Vet Med B 1972;19:598-605.
15. Tomlin J, Pead MJ, Lloyd DH, et al. Methicillin-resistant Staphylococcus aureus infections in 11 dogs. Vet Record 1999;144:60-64.
16. Yasuda R, Kawano J, Onda H, et al. Methicillin-resistant coagulase-negative Staphylococci isolated from healthy horses in Japan; Amer J Vet Res 2000;61:1451-1455.
17. Lee HL. Methicillin (oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl Environm Microbiol 2003;69:6489-6494.
18. Baptiste KE, Williams K, Williams NJ, et al. Methicillin-resistant Staphylococci in companion animals. Emerg Infect Dis 2005;1:1942-1944.
19. Vitale CB, Gross TL, Weese JS. Methicillin-resistant Staphylococcus aureus in cat and owner [letter]. Emerg Infect Dis [serial on the internet] 2006. Available at: http://www.cdc.gov/ncidod/EID/vol12no12/06-0725.htm. Accessed on September 16, 2008.
20. Weese JS, Rousseau J, Traub-Dargatz JL, et al. Community-associated methicillin-resistant Staphylococcus aureus in horses and humans who work with horses. J Amer Vet Med Assoc 2005;226:580-583.
21. Morris DO, Mauldin EA, O'Shea K, et al. Clinical, microbiological, and molecular characterization of methicillin-resistant Staphylococcus aureus infections of cats. Am J Vet Res 2006;67:1421-1425.
22. Wulf M, van Nes A, Eikelenboom-Boskamp A, et al. Methicillin-resistant Staphylococcus aureus in veterinary doctors and students, the Netherlands. Emerg Inf Dis [serial on the internet] 2006. Available at: http://www.cdc.gov/ncidod/EID/vol12no12/06-0355.htm. Accessed on September 16, 2008.
23. Huijsdens XW, van Dijke BJ, Spalburg E, et al. Community-acquired MRSA and pig-farming. Ann Clin Microbiol Antimicrob 2006. Available at: http://www.ann-clinmicrob.com/content/pdf/1476-0711-5-26.pdf . Accessed on September 16, 2008.
24. Manian FA. Asymptomatic nasal carriage of mupirocin-resistant methicillin-resistant Staphylococcus aureus in a pet dog associated with MRSA infection in household contacts. Clin Inf Dis 2003;36:E26-E28.
25. Seguin JC, Walker RD, Caron JP, et al. Methicillin-resistant Staphylococcus aureus outbreak in a veterinary teaching hospital: potential human to animal transmission. J Clin Microbiol 1999;37:1459-1463.
26. De Neeling AJ, Van den Broek MJM, Spalburg EC, Van Santen-Verheuvel MG, Dam-Deisz W, Boshuizen HC, et al. High prevalence of methicillin resistant Staphylococcus aureus in pigs. Vet Microbiol 2007;122:366-372.
27. Lloyd D. Dealing with MRSA in small animal practice. Vet Med Assoc 2006;226: 1855-1863.
28. Weese JS, Rousseau J, Willey BM, et al. Methicillin-resistant Staphylococcus aureus in horses at a veterinary teaching hospital; frequency, characterization and association with clinical disease. J Vet Int Med 2006;20:182-186.
29. Abbott Y, Leonard FC, Markey BK. The prevalence of methicillin-resistant Staphylococcus aureus infection and colonization in companion animals in Ireland. In: Proceedings of the 60th Annual Conference of the Association of Veterinary Teachers and Research Workers, Scarborough. Research in Veterinary Science 2006;Supplement.
30. Voss A, Loeffen F, Bakker J, et al. Methicillin-resistant Straphylococcus aureus in pig farming. Emerg Infect Dis 2005;11:1965-1966.
31. Weese JS, Dick H, Willey BM, et al. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet Microbiol 2006;115:148-155.
32. van Loo IHM, Diederen BMW, Savelkoul PHM, et al. Methicillin-resistant Straphylococcus aureus in meat products, the Netherlands. Emerg Infect Dis 2007;13:1753-1755.
33. Jones TF, Kellum ME, Porter SS, et al. An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. Emerg Inf Dis [serial on the internet] 2002. Available at http://www.cdc.gov/ncidod/eid/vol8no1/01-0174.htm. Accessed on September 16, 2008.
34. Kluytmans J, Van Leeuwen W, Goessens W, et al. Food-initiated outbreak of methicillin-resistant Staphylococcus aureus analyzed by pheno- and genotyping. J Clin Microbiol 1995;33:1121-1128.
35. Bemis DA, Jones RD, Hiatt LE, et al. Comparison of tests to detect oxacillin resistance in Staphylococcus intermedius, Staphylococcus schleiferi, and Staphylococcus aureus isolates from canine hosts. J Clin Microbiol 2006;44:3374-3376.
36. Anderson MEC, Weese JS. Evaluation of a real-time polymerase chain reaction assay for rapid identification of methicillin-resistant Staphylococcus aureus directly from nasal swabs of horses. Vet Microbiol 2007;122:185-189.
37. Weese, 2008a (Weese S. Methicillin resistant Staphyloccoccus aureus. Presented at: The International Conference on Emerging Infectious Diseases: ICEID 2008; March 16-19: Atlanta, GA.)
38. Weese JS. Issues regarding the use of vancomycin in companion animals. J Am Vet Med Assoc 2008b;233:585-587.
39. van Duijkeren E, Wolfhagen MJHM, Box ATA, et al. Human to dog transmission of methicillin-resistant Staphylococcus aureus. Emerg Inf Dis 2004;10:2235-2237.
40. Maree CL, Daum RS, Boyle-Vavra S, et al. Community-associated methicillin-resistant Staphylococcus aureus isolates causing healthcare-associated infections. Emerg Inf Dis 2007;13;236-242.
41. Panlilio AL, Culver DH, Gaynes RP, et al. Methicillin-resistant Staphylococcus aureus in U.S. hospitals, 1975-1992. Infect Control Hosp Epidemiol 1992;13:582-586.
42. Klevens RM, Edwards JR, Tenover FC, et al. Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992-2003. Clin Infect Dis 2006;42:389-391.
43. Johnson AP, Aucken HM, Cavendish S, et al. Dominance of EMRSA-15 and -16 among MRSA causing nosocomial bacteraemia in the UK: analysis of isolates from the European Antimicrobial Resistance Surveillance System (EARSS) [correspondence]. J Antimicrob Chemother 2001;48:143-144.
44. Anderson ME, Lefebvre SL, Weese JS. Evaluation of prevalence and risk factors for methicillin-resistant Staphylococcus aureus colonization in veterinary personnel attending an international equine veterinary conference. Vet Microbiol 2008;166:410-417.
45. Narui K, Takano M, Noguchi N, et al. Susceptibility of methicillin-resistant Staphylococcus aureus isolates to seven biocides. Biol Pharm Bull 2007;30:585-587.
46. Wright JG, Jung S, Holman RC, et al. Infection control practices and zoonotic diseases among veterinarians in the United States. J Am Vet Med Assoc 2008;232:1863-1872.