Staphylococcus pseudintermedius

Staphylococcus pseudintermedius
Scientific classification
Domain: Bacteria
Phylum: Bacillota
Class: Bacilli
Order: Bacillales
Family: Staphylococcaceae
Genus: Staphylococcus
Species:
S. pseudintermedius
Binomial name
Staphylococcus pseudintermedius
Devriese et al. 2005

Staphylococcus pseudintermedius is a gram positive coccus bacteria of the genus Staphylococcus[1] found worldwide.[2] It is primarily a pathogen for domestic animals,[3] but has been known to affect humans as well.[4]S. pseudintermedius is an opportunistic pathogen that secretes immune modulating virulence factors, has many adhesion factors, and the potential to create biofilms, all of which help to determine the pathogenicity of the bacterium.[5][6] Diagnoses of Staphylococcus pseudintermedius have traditionally been made using cytology, plating, and biochemical tests.[7] More recently, molecular technologies like MALDI-TOF, DNA hybridization and PCR have become preferred over biochemical tests for their more rapid and accurate identifications.[8][9] This includes the identification and diagnosis of antibiotic resistant strains.

Morphology and classification

Staphylococci spp. are a genus of gram positive cocci of 0.5 - 1 μm diameter. Staphylococcus pseudintermedius is a non-motile and non-spore forming, facultatively anaerobic bacterium. It appears primarily as grape-like clusters morphologically, but can also be seen as individual or paired cocci.[10] This clustered configuration, as well as the positive catalase test, differentiates staphylococci spp. from streptococci spp., which manifests in chains. Due to its ability to clot blood, S. pseudintermedius subcategorized into a group of coagulase positive (CoPS) staphylococci. CoPS strains typically express more virulence factors. This CoPS characteristic is a contributing factor to its biochemical similarities to S.aureus.[11]

Staphylococcal organisms belong to a more encompassing Staphylococcaceae family of organisms. S. aureus and S. epidermidis are other notable species which fall into the same genus as S. pseudintermedius, under this taxonomic categorization.[11] S. pseudintermedius, S. intermedius, and S. delphini are largely phenotypically indiscriminate and therefore comprise the 'Staphylococcus intermedius group' of organisms.[12] Biochemical properties of these three organisms place them as an intermediate between S. aureus and S. epidermidis.[13]

Staphylococcus pseudintermedius was first identified as a novel species in 2005 using 16S rRNA sequencing of the tRNA intergenic length polymorphisms of the AJ780976 gene loci.[14][15][16] Differing strains of S. pseudintermedius, LMG 22219 - LMG 22222, have been identified in various species: cat, horse, dog, and parrot, respectively.[14] These strains comprise a Staphylococcal species that is distinct from other species within the genus, as distinguished by DNA hybridizations of genome sequences.[12] Previously, many S. pseudintermedius infections or isolates were identified as S. intermedius, before its identification as a distinct taxonomic species.[13]

Isolation of S. pseudintermedius from the skin and mucosa of healthy canine can be between 20-90%, with these frequencies being reduced in healthy felines to 5-45%. It is the most commonly identified Staphylococcal organism in these veterinary species.[13] S. pseudintermedius is classified as a biocontainment risk level 2 organisms due to its moderately pathogenic characteristics.[17]

Diagnosis

Cytology

Using the gram stain technique, Staphylococci are easily identified by their clumped, gram positive, coccus morphology.[7] Slides can be prepared directly using a patient swab, which lends to convenience in the clinic or classroom. However, given that S. pseudintermedius is prevalent within the normal microflora of numerous species, it is better identified as the agent of disease when a corresponding immune reaction is also observed.[7] Where available, the need to identify immune reactors can be avoided by first inoculating the sample onto differential agar plates like SM110,[18] which inhibit the growth of non-staphylococcus bacteria. Cytology alone does not allow for the differentiation between different species in the genus Staphylococci.

Plating

When plated on sheep or bovine blood agar, S. pseudintermedius displays incomplete ß-hemolysis.[19][7] Colonies of S. pseudintermedius on sheep agar are described as medium in size and non-pigmented or grey-white.[19][7] This can be useful for differentiating S. pseudintermedius from coagulase negative Staphylococci, and from S. aureus which tends to be yellow and display more variable hemolytic patterns on agar plates.[19][7] S. pseudintermedius colonies are not hemolytic on equine blood agar.[19][7] Plating is also limited in its ability to identify members of Staphylococci to the species level.

Biochemical tests

Historically, biochemical tests have been an important tool used to discriminate between species of Staphylococci.[19][7] Tests used to identify S. pseudintermedius specifically include DNase,[12] hyaluronidase,[20] coagulase, catalase, and acetoin production tests, amongst others.[7] It can still be difficult to differentiate between members of the S. intermedius group using these methods alone; in veterinary medicine, such diagnoses have relied on the assumption that S. pseudintermedius is the known only member of this group to infect canine skin.[19] More recently, studies using molecular identification methods have found that different S. pseudintermedius strains harbor more phenotypic diversity than previously thought.[8][9][12] It has been speculated that these differences have led to underestimation of the importance of S. pseudintermedius in human skin infections.[21] Further, for this reason, S. pseudintermedius is no longer considered to be reliably identifiable using commercially available biochemical tests alone.[19][8][21] More sensitive methods like MALDI-TOF have therefore since become preferred.[8][9][12]

Identification of methicillin-resistance

Molecular methods, like MALDI-TOF [22] and qPCR primers,[23] are the gold standard for accurately identifying the presence of mecA genes, which confer resistance to Beta-lactam drugs in S. pseudintermedius (a term coined "methicillin-resistance"). However, methicillin-resistance can still be identified reliably using biochemical or phenotypic methods, such as disc diffusion. Although cefoxitin disks have been used,[24] oxacillin disks are considered to be much more sensitive, and thus a more accurate method for predicting methicillin resistance in S. pseudintermedius strains.[25][26]

Epidemiology

In dogs, S. pseudintermedius is normally found on the microflora of the skin.[27][28] The presence of S. pseudintermediushas been observed in higher amounts on dogs that suffer from atopic dermatitis.[28] It is also one of the leading causes of bacterial skin and soft tissue infections,[29][28] such as pyoderma, urinary tract infections,[30] and surgical site infections.[29][2] It is also known to infect cats, although not as common.[31] It is transferred by animal-animal contact, and some dog-human zoonoses have also been reported.[19] Transmission is done either vertically or horizontally.[19] The overall prevalence of S. pseudintermedius in small animals is increasing every year,[32] specifically in small animals worldwide.[29]

Staphylococcus pseudintermedius is becoming a threat due to its heterogeneous qualities[33] and multi-drug resistance phenotype.[2][32] Methicillin-resistant S. pseudintermedius (MRSP) has five major clonal complexe (CC) lineages,[2] each with their own unique traits regarding genetic diversity, geographical distribution and antimicrobial resistance.[34][2] The majority of all MRSP isolates were found in Europe and Asia, with North America, South America, and Oceania contributing only a small portion.[2] The CC71 and CC258 lineages were mostly seen in Europe, CC68 was mostly seen in North America, and CC45 and CC112 seen in Asia.[2] The top three antimicrobials worldwide that MRSP is found to be resistant to are erythromycin, clindamycin, and tetracycline.[2]

When looking at the epidemiology of the Staphylococcus intermedius group (SIG), which includes S. pseudintermedius, S. intermedius, and S. delphini, it is noted that in humans most of the recorded cases were above the age of 50, diabetic, and/or immunocompromised in some way.[35] Most of the cultures came from wound sites and respiratory specimens.[35] S. pseudintermedius is not normally found within the microflora of humans.[19] Humans that work in close proximity to animals are at higher risk of S. pseudintermedius infections, such as veterinarians, animal trainers, and zookeepers.[19] Although the risk of pet owners becoming infected by their pets is low, there have been reported cases.[36]

Pathogenicity and virulence

As previously described, Staphylococcus pseudintermedius, an opportunistic pathogen, is a part of the normal microbiome of skin and mucous membranes in animals.[19] Animals acquire this bacteria through vertical transmission. The strain of S. pseudintermedius colonizing the mother's vaginal mucous membrane is transferred during birth and becomes a part of the offspring's microbiome.[19] A compromised immune system or tissue injury allows this bacteria to push past host defences and create an infection.[19] We then seen clinical manifestations such as purulent dermatitis, otitis externa, conjunctivitis,[6] urinary tract infections,[19] and post-operative infections.[5] Disease is most commonly seen in dogs and cats[19][5] with canine pyoderma being the most notable manifestation of S. pseudintermedius.[37]

The virulence of S. pseudintermedius is an area of on going research and has many unknowns.[38] The virulence factors carried by S. pseudintermedius vary between strains and do not determine if the bacteria will cause an infection. Rather, infection is a result of an animal's immune status,[1] environment, and genetics.[37]

Numerous virulence factors such as enzymes, toxins, and binding proteins have been associated with S. pseudintermedius strains. These include proteases, thermonucleases, coagulases,[38] DNAase, lipase, hemolysin, clumping factor, leukotoxin, enterotoxin,[5] protein A, and exfoliative toxin.[38]

Immune modulating virulence factors

Haemolysins, leukotoxins, exfoliative toxins, and enterotoxins are secreted[19] from the bacteria to modulate the host's immune response.[6]

The pore-forming cytotoxins, α-hemolysin and β-hemolysin, lyse erythrocytes of sheep and rabbits.[19][1] Leukotoxin destroys host leukocytes and causes tissue necrosis.[6] Exfoliative toxin is responsible for the majority of symptoms seen in canine pyoderma[38] and otitis i.e. skin exfoliation and crusting.[6] Exfoliative toxin causes vesicle formation and erosion in epithelial cells resulting in splitting of the skin.[1] Super-antigens such as enterotoxins activate host immune cells causing T cell proliferation and cytokine release.[6] This virulence factor induces vomiting and has been associated with food poisoning in humans.[6] Protein A, an immunoglobulin binding protein, has been found on the surface of S. pseudintermedius.[1] Protein A attaches to the Fc region of host antibodies, rendering them useless. Without the Fc region, the host immune system cannot recognize that antibody; the complement system cannot be activated and phagocytes cannot destroy the bacteria.[6][38]

Virulence factors for dissemination and adhesion

The previously mentioned protein A as well as clumping factor are surface proteins that allow the bacteria to bind to host cells.[19][6] S. pseudintermedius has been found to produce biofilms, an extracellular matrix of protein, DNA, and polysaccharide, which aids the bacteria in avoiding the host immune system and resisting drugs.[5] Biofilms allow the bacteria to persist on medical equipment even after disinfection and adhere to host cells, a component of chronic infections.[5] Fragments of a biofilm can break off and disseminate to other sites in the body, spreading infection.[6] Quorum sensing, a mechanism that coordinates the bacteria's colonization efforts, has been reported in some strains.[19] Coagulase, lipase, and DNAase produced by the bacteria also aid in its dissemination throughout the host body.[6]

Zoonosis

Staphyloccus pseudintermedius has zoonotic potential as it has been found in humans that live with companion animals in the same household.[36][28][19] S. pseudintermedius is not a normal commensal bacterium found in humans, however it is capable of adapting to the human microflora and has become increasingly more common.[19] People whom are at the highest risk for contracting this pathogen are pet owners and veterinarians due to their higher contact with dogs and to a lesser extent cats.[39] The most common place of colonization in the human body is within the nasal cavity and from here, the bacteria can cause infections.[40][41] S. pseudintermedius infections in a human host have been known to cause endocarditis, post-surgical infections, inflammation of the nasal cavity (rhinosinusitis) and catheter-related bacteremia.[5] Staphyloccus pseudintermedius becomes established in a human wound, it has the ability to form antibiotic resistance biofilms.[5] Mechanisms of biofilm resistance of S. pseudintermedius are likely multifactorial and may help to establish infections in humans.[5]

Resistance in humans

There is an increasing prevalence of antibiotic resistance, specifically to methicillin of Staphyloccus pseudintermedius which makes it more challenging to treat when habituating a human host.[42][40][39] Veterinary dermatologists are exposed to animals with skin and soft infections that commonly possess MRSP (methicillin‐resistant Staphylococcus pseudintermedius). Veterinarians have been found to be colonized with MRSP but not MSSP (methicillin‐susceptible S. pseudintermedius).[19][42] Treatment of human MRSP infections is done with antibiotics and these should not be used for treatment in animals.[40] Oral antimicrobial treatment for active infection is commonly done with the use of mupirocin, linezolid, quinupristin, rifampicin or vancomyocin are possible treatments.[40][41] Hand washing, sterilizing equipment and hygiene practices should be implemented to decrease the spread of Staphylococcus infections.[19][41]

References

  1. 1 2 3 4 5 González-Martín M, Corbera JA, Suárez-Bonnet A, Tejedor-Junco MT (December 2020). "Staphylococcus aureus". The Veterinary Quarterly. 40 (1): 118–131. doi:10.1080/01652176.2020.1748253. PMC 7178840. PMID 32223696.
  2. 1 2 3 4 5 6 7 8 Pires Dos Santos T, Damborg P, Moodley A, Guardabassi L (2016). "Staphylococcus pseudintermedius: Inference of Population Structure from Multilocus Sequence Typing Data". Frontiers in Microbiology. 7: 1599. doi:10.3389/fmicb.2016.01599. PMC 5067483. PMID 27803691.
  3. ↑ Vincze S, Paasch A, Walther B, Ruscher C, Lübke-Becker A, Wieler LH, Barbara K (2010). "Multidrug- and methicillin resistant Staphylococcus pseudintermedius as a cause of canine pyoderma: a case report". Berliner und Munchener Tierarztliche Wochenschrift. 123 (9–10): 353–8. PMID 21038805.
  4. ↑ Somayaji R, Priyantha MA, Rubin JE, Church D (August 2016). "Human infections due to Staphylococcus pseudintermedius, an emerging zoonosis of canine origin: report of 24 cases". Diagnostic Microbiology and Infectious Disease. 85 (4): 471–6. doi:10.1016/j.diagmicrobio.2016.05.008. PMID 27241371.
  5. 1 2 3 4 5 6 7 8 9 Pompilio A, De Nicola S, Crocetta V, Guarnieri S, Savini V, Carretto E, Di Bonaventura G (May 2015). "New insights in Staphylococcus pseudintermedius pathogenicity: antibiotic-resistant biofilm formation by a human wound-associated strain". BMC Microbiology. 15: 109. doi:10.1186/s12866-015-0449-x. PMC 4440327. PMID 25994406.
  6. 1 2 3 4 5 6 7 8 9 10 11 Garbacz K, Zarnowska S, Piechowicz L, Haras K (April 2013). "Pathogenicity potential of Staphylococcus pseudintermedius strains isolated from canine carriers and from dogs with infection signs". Virulence. 4 (3): 255–9. doi:10.4161/viru.23526. PMC 3711984. PMID 23328490.
  7. 1 2 3 4 5 6 7 8 9 Becker K, von Eiff C (2011-01-01). "Staphylococcus, Micrococcus, and Other Catalase-Positive Cocci". Manual of Clinical Microbiology, 10th Edition. American Society of Microbiology. pp. 308–330. doi:10.1128/9781555816728.ch19. ISBN 978-1-55581-463-2.
  8. 1 2 3 4 Decristophoris P, Fasola A, Benagli C, Tonolla M, Petrini O (February 2011). "Identification of Staphylococcus intermedius Group by MALDI-TOF MS". Systematic and Applied Microbiology. 34 (1): 45–51. doi:10.1016/j.syapm.2010.11.004. PMID 21300509.
  9. 1 2 3 Murugaiyan J, Walther B, Stamm I, Abou-Elnaga Y, Brueggemann-Schwarze S, Vincze S, et al. (October 2014). "Species differentiation within the Staphylococcus intermedius group using a refined MALDI-TOF MS database". Clinical Microbiology and Infection. 20 (10): 1007–15. doi:10.1111/1469-0691.12662. PMID 24807701.
  10. ↑ Strommenger B, Layer F, Werner G (2018). "Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus in Workers in the Food Industry". Staphylococcus aureus. Elsevier. pp. 163–188. doi:10.1016/b978-0-12-809671-0.00009-7. ISBN 978-0-12-809671-0. PMC 7150186. S2CID 90495265.
  11. 1 2 Chanchaithong P, Prapasarakul N (August 2011). "Biochemical markers and protein pattern analysis for canine coagulase-positive staphylococci and their distribution on dog skin". Journal of Microbiological Methods. 86 (2): 175–81. doi:10.1016/j.mimet.2011.04.019. PMID 21586304.
  12. 1 2 3 4 5 Sasaki T, Kikuchi K, Tanaka Y, Takahashi N, Kamata S, Hiramatsu K (September 2007). "Reclassification of phenotypically identified staphylococcus intermedius strains". Journal of Clinical Microbiology. 45 (9): 2770–8. doi:10.1128/JCM.00360-07. PMC 2045239. PMID 17596353.
  13. 1 2 3 Bond R, Loeffler A (March 2012). "What's happened to Staphylococcus intermedius? Taxonomic revision and emergence of multi-drug resistance". The Journal of Small Animal Practice. 53 (3): 147–54. doi:10.1111/j.1748-5827.2011.01165.x. PMID 22251285.
  14. 1 2 Devriese LA, Vancanneyt M, Baele M, Vaneechoutte M, De Graef E, Snauwaert C, et al. (July 2005). "Staphylococcus pseudintermedius sp. nov., a coagulase-positive species from animals". International Journal of Systematic and Evolutionary Microbiology. 55 (Pt 4): 1569–1573. doi:10.1099/ijs.0.63413-0. PMID 16014483.
  15. ↑ "Staphylococcus pseudintermedius 16S rRNA gene, type strain LMG 22219T". 2005-08-15.
  16. ↑ "Notification that new names and new combinations have appeared in volume 55, part 1, of the IJSEM". International Journal of Systematic and Evolutionary Microbiology. 55 (Pt 3): 987–991. May 2005. doi:10.1099/ijs.0.63740-0. PMID 15879222.
  17. ↑ "Species: Staphylococcus pseudintermedius". lpsn.dsmz.de. Retrieved 2020-11-29.
  18. ↑ "Oxoid - Product Detail". www.oxoid.com. Retrieved 2020-11-21.
  19. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Bannoehr J, Guardabassi L (August 2012). "Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity". Veterinary Dermatology. 23 (4): 253–66, e51–2. doi:10.1111/j.1365-3164.2012.01046.x. PMID 22515504.
  20. ↑ Raus J, Love DN (October 1983). "Characterization of coagulase-positive Staphylococcus intermedius and Staphylococcus aureus isolated from veterinary clinical specimens". Journal of Clinical Microbiology. 18 (4): 789–92. doi:10.1128/JCM.18.4.789-792.1983. PMC 270907. PMID 6630462.
  21. 1 2 Börjesson S, Gómez-Sanz E, Ekström K, Torres C, Grönlund U (April 2015). "Staphylococcus pseudintermedius can be misdiagnosed as Staphylococcus aureus in humans with dog bite wounds". European Journal of Clinical Microbiology & Infectious Diseases. 34 (4): 839–44. doi:10.1007/s10096-014-2300-y. PMID 25532507. S2CID 13173599.
  22. ↑ Nisa S, Bercker C, Midwinter AC, Bruce I, Graham CF, Venter P, et al. (February 2019). "Combining MALDI-TOF and genomics in the study of methicillin resistant and multidrug resistant Staphylococcus pseudintermedius in New Zealand". Scientific Reports. 9 (1): 1271. Bibcode:2019NatSR...9.1271N. doi:10.1038/s41598-018-37503-9. PMC 6361924. PMID 30718644.
  23. ↑ González-Domínguez MS, Carvajal HD, Calle-Echeverri DA, Chinchilla-Cárdenas D (2020-07-23). "Molecular Detection and Characterization of the mecA and nuc Genes From Staphylococcus Species (S. aureus, S. pseudintermedius, and S. schleiferi) Isolated From Dogs Suffering Superficial Pyoderma and Their Antimicrobial Resistance Profiles". Frontiers in Veterinary Science. 7: 376. doi:10.3389/fvets.2020.00376. PMC 7390895. PMID 32793641.
  24. ↑ Wu MT, Burnham CA, Westblade LF, Dien Bard J, Lawhon SD, Wallace MA, et al. (March 2016). "Evaluation of Oxacillin and Cefoxitin Disk and MIC Breakpoints for Prediction of Methicillin Resistance in Human and Veterinary Isolates of Staphylococcus intermedius Group". Journal of Clinical Microbiology. 54 (3): 535–42. doi:10.1128/JCM.02864-15. PMC 4767974. PMID 26607988.
  25. ↑ "Vitek 2 Antimicrobial Susceptibility Testing". Biomedical Safety & Standards. 49 (4): 28. 2019. doi:10.1097/01.bmsas.0000553632.43991.10.
  26. ↑ Jones RN (1984). "NCCLS guidelines: revised performance standards for antimicrobial disk susceptibility tests". Antimicrobic Newsletter. 1 (8): 64–65. doi:10.1016/0738-1751(84)90027-3.
  27. ↑ Davis JA, Jackson CR, Fedorka-Cray PJ, Barrett JB, Brousse JH, Gustafson J, Kucher M (July 2014). "Carriage of methicillin-resistant staphylococci by healthy companion animals in the US". Letters in Applied Microbiology. 59 (1): 1–8. doi:10.1111/lam.12254. PMID 24730724. S2CID 31682652.
  28. 1 2 3 4 Somayaji R, Rubin JE, Priyantha MA, Church D (October 2016). "Exploring Staphylococcus pseudintermedius: an emerging zoonotic pathogen?". Future Microbiology. 11 (11): 1371–1374. doi:10.2217/fmb-2016-0137. PMID 27750440.
  29. 1 2 3 Gagetti P, Wattam AR, Giacoboni G, De Paulis A, Bertona E, Corso A, Rosato AE (July 2019). "Identification and molecular epidemiology of methicillin resistant Staphylococcus pseudintermedius strains isolated from canine clinical samples in Argentina". BMC Veterinary Research. 15 (1): 264. doi:10.1186/s12917-019-1990-x. PMC 6660709. PMID 31351494.
  30. ↑ Couto N, Monchique C, Belas A, Marques C, Gama LT, Pomba C (June 2016). "Trends and molecular mechanisms of antimicrobial resistance in clinical staphylococci isolated from companion animals over a 16 year period". The Journal of Antimicrobial Chemotherapy. 71 (6): 1479–87. doi:10.1093/jac/dkw029. PMID 26944924.
  31. ↑ Kadlec K, Schwarz S, Perreten V, Andersson UG, Finn M, Greko C, et al. (August 2010). "Molecular analysis of methicillin-resistant Staphylococcus pseudintermedius of feline origin from different European countries and North America". The Journal of Antimicrobial Chemotherapy. 65 (8): 1826–8. doi:10.1093/jac/dkq203. PMID 20534627.
  32. 1 2 Eckholm NG, Outerbridge CA, White SD, Sykes JE (February 2013). "Prevalence of and risk factors for isolation of meticillin-resistant Staphylococcus spp. from dogs with pyoderma in northern California, USA". Veterinary Dermatology. 24 (1): 154–61.e34. doi:10.1111/j.1365-3164.2012.01051.x. PMID 23331692.
  33. ↑ Garbacz K, Piechowicz L, Zarnowska S, Haras K, Dabrowska-Szponar M (2011). "Heterogeneity of methicillin-sensitive Staphylococcus pseudintermedius strains isolated from diseased dogs". Polish Journal of Veterinary Sciences. 14 (2): 283–4. doi:10.2478/v10181-011-0043-6. PMID 21721415.
  34. ↑ Osland AM, Vestby LK, Fanuelsen H, Slettemeås JS, Sunde M (April 2012). "Clonal diversity and biofilm-forming ability of methicillin-resistant Staphylococcus pseudintermedius". The Journal of Antimicrobial Chemotherapy. 67 (4): 841–8. doi:10.1093/jac/dkr576. PMID 22258925.
  35. 1 2 Yarbrough ML, Lainhart W, Burnham CA (March 2018). "Epidemiology, Clinical Characteristics, and Antimicrobial Susceptibility Profiles of Human Clinical Isolates of Staphylococcus intermedius Group". Journal of Clinical Microbiology. 56 (3). doi:10.1128/JCM.01788-17. PMC 5824035. PMID 29305548.
  36. 1 2 Kmieciak W, Szewczyk EM (November 2018). "Are zoonotic Staphylococcus pseudintermedius strains a growing threat for humans?". Folia Microbiologica. 63 (6): 743–747. doi:10.1007/s12223-018-0615-2. PMC 6182621. PMID 29804274.
  37. 1 2 Bajwa J (February 2016). "Canine superficial pyoderma and therapeutic considerations". The Canadian Veterinary Journal. 57 (2): 204–6. PMC 4713004. PMID 26834275.
  38. 1 2 3 4 5 Fitzgerald JR (October 2009). "The Staphylococcus intermedius group of bacterial pathogens: species re-classification, pathogenesis and the emergence of meticillin resistance". Veterinary Dermatology. 20 (5–6): 490–5. doi:10.1111/j.1365-3164.2009.00828.x. PMID 20178486.
  39. 1 2 Starlander G, Börjesson S, Grönlund-Andersson U, Tellgren-Roth C, Melhus A (August 2014). "Cluster of infections caused by methicillin-resistant Staphylococcus pseudintermedius in humans in a tertiary hospital". Journal of Clinical Microbiology. 52 (8): 3118–20. doi:10.1128/JCM.00703-14. PMC 4136194. PMID 24871217.
  40. 1 2 3 4 Stegmann R, Burnens A, Maranta CA, Perreten V (September 2010). "Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71". The Journal of Antimicrobial Chemotherapy. 65 (9): 2047–8. doi:10.1093/jac/dkq241. PMID 20601356.
  41. 1 2 3 "Staphylococcal Infections - Infectious Diseases". Merck Manuals Professional Edition. Retrieved 2020-10-06.
  42. 1 2 Paul NC, Moodley A, Ghibaudo G, Guardabassi L (December 2011). "Carriage of methicillin-resistant Staphylococcus pseudintermedius in small animal veterinarians: indirect evidence of zoonotic transmission". Zoonoses and Public Health. 58 (8): 533–9. doi:10.1111/j.1863-2378.2011.01398.x. PMID 21824350. S2CID 36452642.

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