Methicillin-Resistant Staphylococcal Infections: Recent Developments
Christine L. Cain, DVM, Diplomate ACVD
The increasing prevalence of staphylococcal antimicrobial resistance, particularly methicillin resistance, presents a challenge to veterinary practitioners treating clinical infections. Failure to recognize staphylococcal antimicrobial resistance frequently results in ineffective empiric therapeutic choices and protracted clinical disease. In addition, concern is developing regarding potential transmission of antimicrobial-resistant strains from humans to animals and vice versa.
Methicillin-resistant staphylococci possess the mecA gene, carried on the mobile genetic element staphylococcal chromosome cassette mec (SCCmec), which encodes for an altered penicillin-binding protein (PBP2a).
Production of this low-affinity, penicillin-binding protein renders resistance to virtually all beta-lactam derivatives, including:1
- Carbapenems (eg, imipenem, meropenem)
- Cephalosporins (eg, cephalexin, cefpodoxime, cefovecin)
- Penicillins (eg, penicillin, amoxicillin)
- Potentiated penicillins (eg, amoxicillin and clavulanic acid).
Although references to methicillin resistance are commonplace in the medical literature, oxacillin is often used by veterinary microbiology laboratories as the correlate for testing antimicrobial resistance. Both methicillin and oxacillin are semisynthetic penicillinase-resistant penicillins, but oxacillin is more stable in vitro.2,3 Cefoxitin susceptibility testing is also used by human microbiology laboratories to screen for methicillin resistance in Staphylococcus aureus isolates, but may not reliably detect methicillin resistance in S pseudintermedius.2
More recently, a mecA homologue—mecC—has been identified in some European staphylococcal isolates from humans and animals that exhibit methicillin resistance but lack the mecA gene.4-6 The prevalence of this gene in staphylococci is currently unknown.
Although methicillin-resistant staphylococci are not necessarily more virulent than methicillin-susceptible staphylococci,7 treatment options are often severely limited by multidrug resistance. This is particularly true for infections caused by methicillin-resistant S pseudintermedius (MRSP); MRSP isolates are increasingly multidrug resistant.2,8-11
Resistance to non–beta-lactam antimicrobials is common and conveyed by genetic mechanisms other than the mecA gene;2,8-11 these antimicrobials include:
- Potentiated sulfonamides
Due to the prevalence of multidrug resistance in methicillin-resistant strains, empirical switching of antimicrobial classes when treating staphylococcal infections that fail to respond to first-line antimicrobials (particularly beta-lactams) is NOT recommended. Treatment choices should be based on culture and susceptibility testing.
S pseudintermedius colonizes the skin and mucosa of healthy dogs and is the most common cause of canine pyoderma.12 MRSP has been recognized as a cause of pyoderma, surgical site infections (particularly following orthopedic procedures), and urinary tract infections, among others.9,13
Investigators have recently used molecular techniques to classify 3 closely related staphylococcal species—S intermedius, S pseudintermedius, and S delphini—as the S intermedius group. It appears correct to assume that all previously classified S intermedius isolates from dogs, cats, and humans were actually S pseudintermedius isolates.12-15
The prevalence of MRSP infections in veterinary patients has increased substantially over the past decade. Although reported sporadically in the 1990s.16,17 MRSP infections are now commonly reported in the veterinary literature and increasingly isolated by veterinary microbiology laboratories.
MRSP has also been isolated from carriage sites (skin and mucous membranes, including nares, oral mucosa, and rectal mucosa) of healthy dogs and cats.17,18 Several studies support a carriage rate of:
- 1.5% to 3% in healthy dogs19-21
- 0% to 4% in healthy cats.18,22
Overall, the literature suggests that MRSP isolation rates from clinical specimens may significantly exceed the prevalence of MRSP colonization in healthy animals, although prevalence may vary by sampled population and geographic area.
S schleiferi is an emerging cause of infections in veterinary patients.
Two variants have been described based on coagulase production:
- S schleiferi subspecies schleiferi (coagulase negative)
- S schleiferi subspecies coagulans (coagulase positive).
Recent studies suggest the 2 subspecies are not distinct by genotype or clinical behavior; therefore, both should be considered important pathogens.23,24 Coagulase-positive and coagulase-negative S schleiferi are associated with pyoderma (especially recurrent pyoderma) and otitis in dogs with allergic dermatitis, although infections of other body sites in nonallergic dogs have also been reported.24
Methicillin resistance is particularly prevalent in clinical isolates of S schleiferi, with reported rates often exceeding 50%.1,22-26 Fluoroquinolone resistance is also common in methicillin-resistant S schleiferi (MRSS) isolates.9,23,24,27-29
MRSS has been isolated from:
- Dogs and cats with inflammatory skin disease18-20,30-32
- Carriage sites (skin or mucosal) of healthy dogs and cats.
S aureus colonizes approximately 30% of the human population worldwide and is a major cause of skin and soft tissue infections in humans.33 The number of human infections caused by methicillin-resistant S aureus (MRSA) has increased dramatically since the 1960s.34 While human MRSA infections were once primarily nosocomial, community-associated MRSA infections of healthy individuals are being diagnosed more frequently.34,35
MRSA infections have also been reported in a variety of companion and exotic animal species.9,36-41
- In dogs, prevalence of S aureus colonization appears to be substantially lower than that of S pseudintermedius.42 In addition, S aureus infections are far less common than S pseudintermedius infections.9
- In cats, reports conflict as to whether S pseudintermedius or S aureus is the primary colonizing coagulase-positive staphylococcal species.43-46
- Healthy dogs and cats may be colonized by MRSA, although this colonization is likely transient.47,48
As is the case with MRSP, MRSA isolates are often resistant to non–beta-lactam antibiotics, especially:9
MRSA infections in companion and exotic animals are often associated with human hospital- or community-acquired clonal strains, suggesting, but not proving, human-to-animal transmission.38,39,49 Although the possibility of MRSA transmission from colonized or infected humans to animals, or vice versa, has frequently been suggested, the true direction of transmission is difficult to prove.30,49,50 While human-to-animal transmission is usually assumed, the infected or colonized human in the household may not be identified as the MRSA source for the pet.48
The clinical importance of coagulase-negative staphylococci (CoNS), other than the coagulase-negative variant of S schleiferi, has not been well elucidated in veterinary patients. Historically, CoNS were considered commensal organisms or contaminants with limited pathogenic potential; however, they are becoming more frequently associated with nosocomial infections in humans.
CoNS are frequently methicillin resistant and may produce a number of virulence factors.51,52 When CoNS are isolated from clinical specimens, practitioners are encouraged to interpret results in light of culture technique: CoNS isolated from culture samples of closed sites, such as intact pustules or joints, are more likely to be true pathogens than those obtained by swabbing the skin’s surface.
Recent antimicrobial exposure appears to be the most critical risk factor for acquisition of methicillin-resistant staphylococci.13
- In a recent prospective study, Beck and colleagues demonstrated that, following antimicrobial therapy, isolation of MRSP from the skin and mucosal sites of dogs with pyoderma caused by methicillin-susceptible S pseudintermedius (MSSP) is common.13
- Similarly, in a large retrospective study, recent administration of beta-lactam antimicrobials was found to be a risk factor for dogs with MRSS clinical isolates.24
- Recent administration of beta-lactams or fluoroquinolones is a risk factor for MRSA infection in dogs and cats.37,53
Additional risk factors for MRSA infection include:37,53
- Contact with ill or hospitalized human
- Intravenous catheterization
- Multiple antimicrobial courses
- Prolonged hospitalization
- Surgical implants.
It is likely that alteration of commensal staphylococcal flora by systemic antimicrobial treatment, particularly beta-lactam antibiotics, allows for subsequent colonization by methicillin-resistant strains. With the increasing prevalence of antimicrobial resistant strains, practitioners are encouraged to consider the potential for infection associated with methicillin-resistant staphylococci even in the absence of risk factors, such as recent antimicrobial administration or hospitalization.
CULTURE & SUSCEPTIBILITY
Given the increasing prevalence of methicillin- and multidrug-resistant staphylococci, culture and susceptibility testing (Figure 1) is likely an underutilized tool, particularly in the management of pyoderma, urinary tract infections, wounds, and surgical site infections.
Clinical indications for performing culture and susceptibility testing include:
- Clinical lesions consistent with deep pyoderma, such as furuncles, nodules, and draining tracts
- Any surgical site infection, particularly those associated with orthopedic procedures13,54
- Presence of a nonhealing wound
- Cytologic evidence of mixed or nonstaphylococcal infection (eg, intracellular bacterial rods)
- History of prior antimicrobial-resistant staphylococcal infection
- History of recent antimicrobial therapy
- Lack of response to appropriate empiric antimicrobial therapy
- Recurrent or relapsing infection.
Inducible Resistance & Clindamycin
- Inducible resistance, in which the presence of an inducing agent, such as erythromycin, promotes expression of a resistant phenotype, has been reported in MRSA isolates from humans and animals and some MRSP isolates.56,57
- Clindamycin use in infections caused by isolates exhibiting inducible resistance may result in treatment failure.56,57
- Microbiology laboratories can test for inducible clindamycin resistance using a double disk diffusion test (D-test) with adjacent erythromycin and clindamycin disks (Figure 2).
- In the absence of this test, clinicians may predict inducible resistance based on susceptibility results, indicating erythromycin resistance and clindamycin susceptibility.56
Despite the importance of culture and susceptibility testing in management of staphylococcal infections, empiric antimicrobial therapy remains common practice for first-time infections or treatment-naïve patients, especially patients with pyoderma.
- Beta-lactam derivatives, especially cephalosporins, are frequently considered first-line choices in treatment of pyoderma due to their bactericidal activity, tissue penetration, and low incidence of adverse effects.55
- Preferential selection of other antimicrobials, such as macrolides, lincosamides, or potentiated sulfonamides, as first-line therapies for staphylococcal infections has been suggested due to concerns regarding potential colonization with methicillin-resistant strains due to beta-lactam antimicrobial use.24 Due to frequent resistance in methicillin-resistant strains, especially MRSP, practitioners should be aware for the potential of empiric failure with these antimicrobials; changes in therapy should be based on culture and susceptibility results.
- Use of systemic fluoroquinolones for treatment of staphylococcal infections should be reserved for cases in which:
- In vitro susceptibility is demonstrated
- A fluoroquinolone is considered the most appropriate antimicrobial choice for the patient.
Empiric use of fluoroquinolones is NOT recommended due to the potential for therapeutic failure if the infection is caused by methicillin-resistant strains, which frequently exhibit coresistance to fluoroquinolones.
Due to the connection between systemic antimicrobial therapy and acquisition of methicillin-resistant strains, topical antimicrobial or antiseptic therapy for the treatment of canine pyoderma, especially for first-time, mild, or localized infections, is recommended.31
RESISTANT INFECTION THERAPY
Table 1 lists antimicrobial options and dosing regimens for methicillin-resistant staphylococcal pyoderma, based on culture and susceptibility.
Recommended treatment duration for methicillin-resistant staphylococcal infections does not necessarily exceed that recommended for methicillin-susceptible infections, which is the case, for example, for methicillin-susceptible staphylococcal pyoderma:58
- Superficial infections should be treated for a minimum of 3 to 4 weeks; then 1 week past clinical resolution
- Deep infections should be treated for a minimum of 6 to 8 weeks; then 2 weeks past clinical resolution.
Clinical resolution of MRSP-associated pyoderma may take longer than resolution of MSSP-associated pyoderma, but this is more likely due to empiric treatment failure, infection chronicity, or secondary pathologic changes to the skin rather than increased virulence of methicillin-resistant strains.59
Systemic antimicrobial options for treatment of methicillin- and multidrug-resistant staphylococcal infections are often limited to:
- Aminoglycosides, particularly amikacin
When prescribed for extended therapy, potential adverse effects of these medications must be considered (see Table 2).
Despite good in vitro susceptibility,8 administration of antimicrobials used in humans for serious MRSA infections, such as linezolid and vancomycin,60 should be avoided in veterinary patients due to ethical concerns (these drugs are reserved for use in humans with MRSA infections); cost of these medications is also prohibitive.61,62
Topical antimicrobial therapy for resistant staphylococcal infections has increased due to:
- Limited options for systemic therapy
- Potential for adverse drug effects
- Rise of multidrug resistance.
Topical therapy alone has been found to be effective for treatment of pyoderma associated with methicillin-resistant staphylococci (Figures 3 and 4).59 Therapeutic options for sole or adjunctive therapy include:63
- Hypochlorous acid and sodium hypochlorite based products (including dilute bleach baths)
- Mupirocin (2%) ointment
- Shampoos, conditioners, sprays, and wipes containing chlorhexidine (2%–4%), benzoyl peroxide, or ethyl lactate
- Wipes containing nisin, an antimicrobial protein.
Methicillin- and multidrug-resistant staphylococcal infections are becoming increasingly common in veterinary patients.
- Empiric antimicrobial selection is difficult and treatment failure is common.
- Culture and susceptibility testing is indicated for management of staphylococcal infections, particularly canine pyoderma and surgical site infections.
- Topical antimicrobial therapy may be useful for infection treatment and prevention in cases of limited systemic antimicrobial options or adverse drug effects.
- StriStct hygiene practices should be observed to limit bacterial transmission.
Strict hygiene practices are critical to limit transmission of methicillin-resistant staphylococci. Prudent hygiene practices include:7,48,64-67
- Barrier precautions, such as disposable gloves, when working with infected patients
- Covering open or draining wounds
- Frequent cleaning of dishes, washing of bedding, and environmental disinfection
- Regular hand washing, especially after handling infected patients and between patients
- Restricting infected pets from sleeping in bed with humans (or vice versa) and preventing pets from licking humans.
To learn more about preventing spread of infection, read Practical Strategies for Preventing Nosocomial Infections (March/April 2013 issue of Today’s Veterinary Practice), available at todaysveterinarypractice.com.
CoNS = coagulase-negative staphylococci; MRSA = methicillin-resistant Staphylococcus aureus; MRSP = methicillin-resistant Staphylococcus pseudintermedius; MRSS = methicillin-resistant Staphylococcus schleiferi; MSSP = methicillin-susceptible Staphylococcus pseudintermedius
- Kania SA, Williamson NL, Frank LA, et al. Methicillin resistance of staphylococci isolated from the skin of dogs with pyoderma. Am J Vet Res 2004; 65:1265-1268.
- Bemis DA, Jones RD, Frank LA, et al. Evaluation of susceptibility test breakpoints used to predict mecA-mediated resistance in Staphylococcus pseudintermedius isolated from dogs. J Vet Diagn Invest 2009; 21:53-58.
- Cole LK, Kwochka KW, Hillier A, et al. Identification of oxacillin-resistant staphylococci in dogs with end-stage otitis. Vet Rec 2006; 159:418-419.
- Medhus A, Slettemehas JS, Marstein L, et al. Methicillin-resistant Staphylococcus aureus with the novel mecC gene variant from a cat suffering from chronic conjunctivitis. J Antimicrob Chemother 2012; 0:1-2.
- Kriegskorte A, Ballhausen B, Idelevich EA, et al. Human MRSA isolates with novel genetic homolog, Germany [letter to the editor]. Emerg Infect Dis 2012; 18:1016-1018.
- Paterson GK, Larsen AR, Robb A, et al. The newly described mecA homologue, mecALGA251, is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species. J Antimicrob Chemother 2012; 67:2809-2813.
- Cohn LA, Middleton JR. A veterinary perspective on methicillin-resistant staphylococci. J Vet Emerg Crit Care 2010; 20:31-45.
- Ruscher C, Lubke-Becker A, Semmler T, et al. Widespread rapid emergence of a distinct methicillin- and multidrug-resistant Staphylococcus pseudintermedius (MRSP) genetic lineage in Europe. Vet Microbiol 2010; 144:340-346.
- Morris DO, Rook KA, Shofer FS. Screening of Staphylococcus aureus, Staphylococcus intermedius, and Staphylococcus schleiferi isolates obtained from small companion animals for antimicrobial resistance: A retrospective review of 749 isolates (2003-04). Vet Dermatol 2006; 17:332-337.
- Loeffler A, Linek M, Moodley A, et al. First report of multiresistant, mecA-positive Staphylococcus intermedius in Europe: 12 cases from a veterinary dermatology referral clinic in Germany. Vet Dermatol 2007; 18:412-421.
- Kadlec K, Schwarz S, Perreten V, et al. Molecular analysis of methicillin-resistant Staphylococcus pseudintermedius of feline origin from different European countries and North America. J Antimicrob Chemother 2010; 65:1826-1837.
- Sasaki T, Kikucki K, Tanaka Y, et al. Reclassification of phenotypically identified Staphylococcus intermedius strains. J Clin Microbiol 2007; 45:2770-2778.
- Weese JS, Faires MC, Frank LA, et al. Factors associated with methicillin-susceptible and methicillin-resistant Staphylococcus pseudintermedius infection in dogs. JAVMA 2012; 240:1450-1455.
- Bannoehr J, Ben Zakour NL, Waller AS, et al. Population genetic structure of the Staphylococcus intermedius group: Insights into agr diversification and the emergence of methicillin-resistant strains. J Bacteriol 2007; 189:8685-8692.
- Fitzgerald JR. The Staphylococcus intermedius group of bacterial pathogens: Species re-classification, pathogenesis and the emergence of meticillin resistance. Vet Dermatol 2009; 20:490-495.
- Piriz S, Valle J, Mateos EM, et al. In vitro activity of fifteen antimicrobial agents against methicillin-resistant and methicillin-susceptible Staphylococcus intermedius. J Vet Pharmacol Therap 1996; 19:118-123.
- Gortel K, Campbell KL, Kakoma I, et al. Methicillin resistance among staphylococci isolated from dogs. Am J Vet Res 1999; 60:1526-1530.
- Abraham JL, Morris DO, Griffeth GC, et al. Surveillance of healthy cats and cats with inflammatory skin disease for colonization of the skin by methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi ssp. schleiferi. Vet Dermatol 2007; 18:252-259.
- Griffeth GC, Morris DO, Abraham JL, et al. Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Vet Dermatol 2008; 19:142-149.
- Hanselman BA, Kruth S, Weese JS. Methicillin-resistant staphylococcal colonization in dogs entering a veterinary teaching hospital. Vet Microbiol 2008; 126:277-281.
- Gingrich EN, Kurt T, Hyatt DR, et al. Prevalence of methicillin-resistant staphylococci in northern Colorado shelter animals. J Vet Diagn Invest 2011; 23:947-950.
- Couto N, Pomba C, Moodley A, et al. Prevalence of meticillin-resistant staphylococci among dogs and cats at a veterinary teaching hospital in Portugal. Vet Rec 2011;169: 72.
- Cain CL, Morris DO, O’Shea K, et al. Genotypic relatedness and phenotypic characterization of Staphylococcus schleiferi subspecies in clinical samples from dogs. J Vet Res 2011; 72:96-102.
- Cain CL, Morris DO, Rankin SC. Clinical characterization of Staphylococcus schleiferi infections and identification of risk factors for acquisition of oxacillin-resistant strains in dogs: 225 cases (2003-2009). JAVMA 2011; 239:1566-1573.
- Frank LA, Kania SA, Hnilica KA, et al. Isolation of Staphylococcus schleiferi from dogs with pyoderma. JAVMA 2003; 222:451-454.
- 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.
- Kawakami T, Shibata S, Murayama N, et al. Antimicrobial susceptibility and methicillin resistance in Staphylococcus pseudintermedius and Staphylococcus schleiferi subsp. coagulans isolated from dogs with pyoderma in Japan. J Vet Med Sci 2010; 72:1615-1619.
- Vanni M, Tognetti R, Pretti C, et al. Antimicrobial susceptibility of Staphylococcus intermedius and Staphylococcus schleiferi isolated from dogs. Res Vet Sci 2009; 87:192-195.
- Intorre L, Vanni M, Di Bello D, et al. Antimicrobial susceptibility and mechanism of resistance to fluoroquinolones in Staphylococcus intermedius and Staphylococcus schleiferi. J Vet Pharmacol Therap 2007; 30:464-469.
- Morris DO, Boston RC, O’Shea K, et al. The prevalence of carriage of meticillin-resistant staphylococci by veterinary dermatology practice staff and their respective pets. Vet Dermatol 2010; 21:400-407.
- Beck KM, Waisglass SE, Dick HLN, et al. Prevalence of meticillin-resistant Staphylococcus pseudintermedius (MRSP) from skin and carriage sites of dogs after treatment of their meticillin-resistant or meticillin-sensitive staphylococcal pyoderma. Vet Dermatol 2012; 23:369-375.
- May ER, Kinyon JM, Noxon JO. Nasal carriage of Staphylococcus schleiferi from healthy dogs and dogs with otitis, pyoderma or both. Vet Microbiol 2012; 160:443-448.
- Tang YW, Stratton CW. Staphylococcus aureus: An old pathogen with new weapons. Clin Lab Med 2010; 30:179-208.
- Ippolito G, Leone S, Lauria FN, et al. Methicillin-resistant Staphylococcus aureus: The superbug. Int J Infect Dis 2010; 14S4:S7-S11.
- Duquette RA, Nuttall TJ. Methicillin-resistant Staphylococcus aureus in dogs and cats: An emerging problem? J Small Anim Pract 2004; 45:591-597.
- Middleton JR, Fales WH, Luby CD, et al. Surveillance of Staphylococcus aureus in veterinary teaching hospitals. J Clin Microbiol 2005; 43:2916-2919.
- Faires MC, Traverse M, Tater KC, et al. Methicillin-resistant and -susceptible Staphylococcus aureus infections in dogs. Emerg Infect Dis 2010; 16:69-75.
- Rankin S, Roberts S, O’Shea K, et al. Panton valentine leukocidin (PVL) toxin positive MRSA strains isolated from companion animals. Vet Microbiol 2005; 108:145-148.
- Walther B, Wieler LH, Friedrich AW, et al. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from small and exotic animals at a university hospital during routine microbiological examinations. Vet Microbiol 2008; 127:171-178.
- Briscoe JA, Morris DO, Rankin SC, et al. Methicillin-resistant Staphylococcus aureus-associated dermatitis in a Congo African Grey Parrot. J Avian Med Surg 2008; 22:336-343.
- Centers for Disease Control and Prevention. Methicillin-resistant Staphylococcus aureus skin infections from an elephant calf—San Diego, California, 2008. Morb Mortal Wkly Rep 2009; 58:194-198.
- Fazakerley J, Nuttall T, Sales D, et al. Staphylococcal colonization of mucosal and lesional skin sites in atopic and healthy dogs. Vet Dermatol 2009; 20:179-184.
- Cox HU, Hoskins JD, Newman SS, et al. Distribution of staphylococcal species on clinical normal cats. Am J Vet Res 1985; 46:1824-1828.
- Igimi S, Atobe H, Tohya Y, et al. Characterization of the most frequently encountered Staphylococcus sp. in cats. Vet Microbiol 1994; 39:255-260.
- Lilenbaum W, Nunes ELC, Azeredo MAI. Prevalence and antimicrobial susceptibility of staphylococci isolated from the skin surface of clinically normal cats. Lett Appl Microbiol 1998; 27:224-228.
- Lilenbaum W, Esteves AL, Souza GN. Prevalence and antimicrobial susceptibility of staphylococci isolated from saliva of clinically normal cats. Lett Appl Microbiol 1998; 28:448-452.
- Loeffler A, Pfeiffer DU, Lindsay JA, et al. Lack of transmission of methicillin-resistant Staphylococcus aureus (MRSA) between apparently healthy dogs in a rescue kennel 2010; Vet Microbiol 141:178-181.
- Morris DO, Lautenbach E, Zaoutis T, et al. Potential for pet animals to harbour methicillin-resistant Staphylococcus aureus when residing with human MRSA patients. Zoonoses Public Health 2012; 59:286-293.
- 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.
- Faires MC, Tater KC, Weese JS. An investigation of methicillin-resistant Staphylococcus aureus colonization in people and pets in the same household with an infected person or infected pet. JAVMA 2009; 235:540-543.
- Piette A, Verschraegen G. Role of coagulase-negative staphylococci in human disease. Vet Microbiol 2009; 134:45-54.
- von Eiff C, Peters G, Heilmann C. Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2002; 2:677-685.
- Magalhaes RJS, Loeffler A, Lindsay J, et al. Risk factors for methicillin-resistant Staphylococcus aureus (MRSA) infection in dogs and cats: A case-control study. Vet Res 2010; 41:55.
- Weese JS. A review of multidrug resistant surgical site infections. Vet Comp Orthop Traumatol 2008; 21: 1-7.
- Mason IS, Kietzmann M. Cephalosporins—pharmacologic basis of clinical use in veterinary dermatology. Vet Dermatol 1999; 10:187-192.
- Rich M, Deighton L, Roberts L. Clindamycin-resistance in methicillin-resistant Staphylococcus aureus isolated from animals. Vet Microbiol 2005; 111:237-240.
- Faires M, Gard S, Aucoin D, et al. Inducible clindamycin-resistance in methicillin-resistant Staphylococcus aureus and methicillin-resistant Staphylococcus pseudintermedius isolates from and cats [letter to the editor]. Vet Microbiol 2009; 139:419-420.
- Ihrke PJ. Bacterial infections of the skin. In Greene CE (ed): Infectious Diseases of the Dog and Cat, 3rd ed. St. Louis: Saunders Elsevier, 2006, pp 807-815.
- Bryan J, Frank LA, Rohrbach BW, et al. Treatment outcome of dogs with meticillin-resistant and meticillin-susceptible Staphylococcus pseudintermedius pyoderma. Vet Dermatol 2012; 23:361-368.
- Liu C, Bayer A, Cosgrove SE, et al. Clinical practice guidelines by the infectious diseases society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children: Executive summary. Clin Infect Dis 2011; 52:285-292.
- Perreten V, Kadlec K, Schwarz S, et al. Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: An international multicentre study. J Antimicrob Chemother 2010; 65:1145-1154.
- Papich MG. Selection of antibiotics for meticillin-resistant Staphylococcus pseudintermedius: Time to revisit old drugs? Vet Dermatol 2012; 23:352-360.
- Jeffers JG. Topical therapy for drug-resistant pyoderma in small animals. Vet Clin North Am Small Anim Pract 2013; 43:41-50.
- Hanselman BA, Kruth SA, Rousseau J, et al. Coagulase positive staphylococcal colonization of humans and their household pets. Can Vet J 2009; 50:954-958.
- Lefebvre SL, Reid-Smith RJ, Waltner-Toews D, et al. Incidence of acquisition of methicillin-resistant Staphylococcus aureus, Clostridium difficile, and other health-care associated pathogens by dogs that participate in animal-assisted interventions. JAVMA 2009; 234:1404-1417.
- Weese JS, Faires M, Rousseau J, et al. Cluster of methicillin-resistant Staphylococcus aureus colonization in a small animal intensive care unit. JAVMA 2007; 231:1361-1364.
- Walther B, Hermes J, Cuny C, et al. Sharing more than friendship—nasal colonization with coagulase-positive staphylococci (CPS) and co-habitation aspects of dogs and their owners. PLoS One 2012; 7:E35197.