Staphylococcus schleiferi is a Gram-positive, cocci-shaped bacterium of the family Staphylococcaceae. It is facultatively anaerobic, coagulase-variable, and can be readily cultured on blood agar where the bacterium tends to form opaque, non-pigmented colonies and beta (β) hemolysis. There exists two subspecies under the species S. schleiferi: Staphylococcus schleiferi subsp. schleiferi (coagulase negative) and Staphylococcus schleiferi subsp. coagulans (coagulase positive).
Staphylococcus schleiferi is commonly recognized as a veterinary pathogen affecting household pets, but has not been identified as a disease causing organism in large animals. S. schleiferi has been identified as a causative agent of conditions of Pyoderma, Otitis Externa, and Otitis media in both dogs and cats; although more commonly causing inflammatory conditions in dogs than in cats. Human infections have been described in some case reports, resulting in certain disease conditions including: surgical site infections, pediatric meningitis, endocarditis, and intravascular device-related bacteremia. Although both companion animals and humans can acquire disease from this organism, its zoonotic potential is not well understood. Antimicrobial therapy has been generally successful in treatment of infections, however, resistance to beta-lactam antibiotics have been reported, resulting in persistent infections for both humans and veterinary species.
Since its first description in 1988, little has been reported regarding the pathogenicity and virulence of Staphylococcus schleiferi. However, similarities with infections caused by Staphylococcus aureus suggest that the two species may also share similar determinants of virulence. Virulence factors associated with S. schleiferi have been identified to include the production of fatty acid modifying enzyme (FAME), biofilms, penicillin-binding protein 2a (PBP2a), as well as various enterotoxins and exoenzymes.
Staphylococcus schleiferi is differentiated from other Staphylococcal species based on their coagulation reaction, but because there is a coagulase positive and a coagulase negative subspecies of S. schleiferi, additional biochemical tests are required. These tests are often not done clinically as treatment is based on susceptibility testing and location of the infection.
Microbiology
History and taxonomy In 1988, Freney et al. isolated two previously unidentified Staphylococcus species from human clinical specimens: S. schleiferi and S. lugdunensis. The former species was named schleiferi in honor of German microbiologist Karl Heinz Schleifer, to mark his significant contributions to the taxonomy of gram-positive bacteria. Later in 1990, a coagulase-positive subtype was isolated from dogs and cats by Igimi et al. This led to the classification of Staphylococcus schleiferi into two distinct subspecies, the coagulase-negative S. schleiferi schleiferi and the coagulase-positive S. schleiferi coagulans. Both S. schleiferi subspecies have since been reported to be linked to an array of infections in humans and companion animals.
Cellular morphology
Staphylococcus schleiferi is a facultatively anaerobic, coagulase-variable, Gram-positive cocci organism. It is nonmotile and nonspore-forming. When cultured on 5% sheep blood agar, isolates of S. schleiferi form circular, opaque, non-pigmented colonies of approximately 0.8 to 1.0μm in diameter. A complete (β) hemolysis can be seen on blood agar as well. On a Gram stain, S. schleiferi appears as individuals, pairs, small clusters, or chains of 3 to 7 cells.
Biochemistry and identification Staphylococcus schleiferi can be readily identified using matrix-assisted laser desorption ionization time of flight (MALDI-TOF), although differentiation to the subspecies level often requires biochemical testing with tube coagulase and urease reactions. S. schleiferi subspecies schleiferi tests negative for tube coagulase and urease, whereas S. schleiferi subspecies coagulans tests positive for tube coagulase and urease. Commercial identification systems often recommend the use of additional biochemical tests to further confirm an identification of S. schleiferi.
Differentiation from Staphylococcus aureus
Staphylococcus schleiferi can often be mistaken for Staphylococcus aureus as both staphylococcal species produce heat-stable DNase and clumping factor. Moreover, colonies of S. aureus appear morphologically similar when grown on blood agar. Many have even suggested that there is an underestimation of reported S. schleiferi infections due to false identifications of S. schleiferi as S. aureus. Multiple biochemical tests can be performed to differentiate these related Staphylococcus species, although some analyses, such as the tube coagulase test, are not performed in routine laboratory procedures. Sugar fermentation tests, for instance, can be performed as S. schleiferi does not acidify maltose, mannitol, or sucrose, as opposed to S. aureus. S. schleiferi also demonstrates pyrrolidonyl arlamidase (PYR) activity, whereas S. aureus tests negative for PYR enzymatic activity. S. schleiferi can also be discerned from S. aureus by production of a different thermonuclease that lacks pigmentation. In contrast to S. schleiferi which produces β-hemolysin and consequently exhibits a complete (β) hemolysis, strains of S. aureus can produce double-zone (α + β) hemolysis.
Differentiation from Staphylococcus lugdunensis Although Staphylococcus schleiferi and Staphylococcus lugdunensis both demonstrate PYR activity and production of clumping factor, these staphylococcal species can be differentiated in their different hemolytic activities on blood agar. While S. schleiferi presents a complete (β) hemolysis, S. lugdunensis produces a double-zone (α + β) hemolysis. S. schleiferi is also capable of adherence to glass, while S. lugdunensis fails to adhere to glass.
Epidemiology
Prevalence Staphylococcus schleiferi is recognized as commensal microflora on the skin of humans and animals like many other Staphylococci species. It is more commonly recognized as a veterinary pathogen affecting household pets; in particular, S. schleiferi has been isolated from healthy dogs as well as dogs with skin and ear infections.
Staphylococcus schleiferi is less commonly associated with human infection, but can be nosocomial acquired. A study performed at a tertiary care centre in Northern Spain found that out of 28 patients documented with S. schleiferi infection, 89.3% were men. Over half of the patients that were infected also had some degree of immunosuppression, namely malignant neoplasm. Most infections were also related to wound-infection (mainly surgical-site infections) - however, infection-related mortality was low.
Geographical distribution Staphylococcus schleiferi has a worldwide distribution. This opportunistic pathogen has been isolated from dogs with pyoderma and otitis externa in Korea, Japan, France, Italy, and the West Indies. . S. schleiferi was the second most prevalent species present in samples collected from dogs with pyoderma and otitis externa in Korea. It has also been isolated from 36 patients in northern Spain from 1993-1999.
Staphylococcus schleiferi was isolated from a multitude of pinniped species and penguins in the Antarctic and Scotland.
Antimicrobial resistance
Methicillin-resistance Methicillin-resistant staphylococci is a growing public health concern, with systemic use of antibiotics becoming more common. Systemic antibiotic use has been associated with the development of infections with MR staphylococci. Increased prevalence of methicillin-resistant staphylococci has been reported in specialty dermatology practices in the United States and in Canada. A study performed at University of Pennsylvania School of Veterinary Medicine found that 40% of S. schleiferi were resistant to methicillin. At the University of Tennessee, 46.6% of the S. schleiferi isolated were resistant to oxacillin. Seven strains of methicillin-resistant S. schleiferi (MRSS) were also isolated from dogs presenting with pyoderma and otitis externa in Korea.
Compared to other MR staphylococci, MRSS maintained the most favourable susceptibility profile. However, to avoid selecting for resistant strains, culture and susceptibility testing is crucial prior to starting a course of treatment.
Fluoroquinolone resistance Eight isolates of S. schleiferi from canine patients were tested against 23 antimicrobial agents. 62.5% showed resistance to multiple fluoroquinolones. A similar study found only 40% of S. schleiferi isolates to be susceptible to all 16 fluoroquinolones tested against it.
Although the current antimicrobials commonly used for treatment of S. schleiferi caused infections experimentally show susceptibility, the changes in temporal trends and different resistance patterns for S. schleiferi emphasize the importance of antimicrobial susceptibility testing to choose the most appropriate treatment of infections.
Zoonotic potential Staphylococcus species were initially thought to be host-specific pathogens, however, human strains of S. intermedius, S. schleiferi, and S. aureus have been isolated from animal reservoirs, indicating their multi-host potential. S. schleiferi is a known canine skin pathogen, causing pyoderma, otitis externa, and otitis media in healthy dogs with no pre-existing risk factors; and has also been reported to infect humans, causing a multitude of nosocomial infections such as endocarditis, osteomyelitis, septic arthritis, UTIs, and wound infections. It is unknown what role zoonotic transmission has in human disease acquisition associated with S. schleiferi, however, there is growing evidence of zoonoses occurring with other related Staphylococcus species.
Evidence of zoonosis in Staphylococcus species
Staphylococcus aureus Methicillin-Resistant S. aureus (MRSA) has been a growing public health concern, with increases in infection prevalence in individuals with no apparent risk factors. Both zoonotic and reverse zoonotic transmission have been reported for MRSA, indicating the ability for the bacteria to accumulate on animal reservoirs, and to reinfect humans.
Staphylococcus intermedius S. intermedius is a common commensal of dogs and cats, though rarely causes infections in humans. However, infections have been found in people with relation to household pets, resulting in a report of postoperative sinus infection, otitis externa, bite wounds, catheter related injuries, and surgery. Owners of dogs affected by deep pyoderma carried multiple anti-microbial resistant strains of S. intermedius which is thought to be transferred between the canine and human pathogenic staphylococci.
Staphylococcus pseudintermedius S. pseudintermedius is considered a novel species of Staphylococcus, and is a commensal organism found on the skin and mucous membranes of dogs. Transmission from canines is suspected to cause skin and soft tissue infections in people. S. pseudintermedius was also isolated from skin breaks of child with eczema following licking from the family dog.
Staphylococcus schleiferi Although there is little evidence outlining the incidence of zoonotic transmission, the increasing recognition of Methicillin-Resistant isolates of S. schleiferi may have importance to public health, as there is already concern regarding possible transfer of resistance genes from canine to human staphylococci species.
Virulence The mechanisms that Staphylococcus schleiferi employ to carry out its virulence are not well elucidated however, similarities between infections of S. schleiferi and other Staphylococcus spp. such as Staphylococcus aureus suggest that these species also share similar determinants of virulence.
Fatty acid modifying enzyme (FAME) and lipase