Biology:Staphylococcus pseudintermedius

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Short description: Species of bacterium

Staphylococcus pseudintermedius
Scientific classification edit
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.[citation needed] Staphylococcus pseudintermedius is a non-motile and non-spore forming, facultatively anaerobic bacterium.[citation needed] It appears primarily as grape-like clusters morphologically, but can also be seen as individual or paired cocci.[10][citation needed] 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.[citation needed] 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] While plating may help differentiate species, biochemical or DNA testing may be necessary.[20]

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,[21] 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.[22] Further, for this reason, S. pseudintermedius is no longer considered to be reliably identifiable using commercially available biochemical tests alone.[19][8][22] More sensitive methods like MALDI-TOF have therefore since become preferred.[8][9][12]

Identification of methicillin-resistance

Molecular methods, like MALDI-TOF [23] and qPCR primers,[24] 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,[25] oxacillin disks are considered to be much more sensitive, and thus a more accurate method for predicting methicillin resistance in S. pseudintermedius strains.[26][27]

Epidemiology

In dogs, S. pseudintermedius is normally found on the microflora of the skin.[28][29] The presence of S. pseudintermediushas been observed in higher amounts on dogs that suffer from atopic dermatitis.[29] It is also one of the leading causes of bacterial skin and soft tissue infections,[30][29] such as pyoderma, urinary tract infections,[31] and surgical site infections.[30][2] It is also known to infect cats, although not as common.[32] 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,[33] specifically in small animals worldwide.[30]

Staphylococcus pseudintermedius is becoming a threat due to its heterogeneous qualities[34] and multi-drug resistance phenotype.[2][33] 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.[35][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.[36] Most of the cultures came from wound sites and respiratory specimens.[36] 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.[37]

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.[38]

The virulence of S. pseudintermedius is an area of on going research and has many unknowns.[39] 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.[38]

Numerous virulence factors such as enzymes, toxins, and binding proteins have been associated with S. pseudintermedius strains. These include proteases, thermonucleases, coagulases,[39] DNAase, lipase, hemolysin, clumping factor, leukotoxin, enterotoxin,[5] protein A, and exfoliative toxin.[39]

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[39] 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][39]

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.[37][29][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.[40] The most common place of colonization in the human body is within the nasal cavity and from here, the bacteria can cause infections.[41][42] 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.[43][41][40] 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][43] Treatment of human MRSP infections is done with antibiotics and these should not be used for treatment in animals.[41] Oral antimicrobial treatment for active infection is commonly done with the use of mupirocin, linezolid, quinupristin, rifampicin or vancomyocin are possible treatments.[41][42] Hand washing, sterilizing equipment and hygiene practices should be implemented to decrease the spread of Staphylococcus infections.[19][42]

References

  1. ↑ 1.0 1.1 1.2 1.3 1.4 "Staphylococcus aureus". The Veterinary Quarterly 40 (1): 118–131. December 2020. doi:10.1080/01652176.2020.1748253. PMID 32223696. 
  2. ↑ 2.0 2.1 2.2 2.3 2.4 2.5 2.6 2.7 "Staphylococcus pseudintermedius: Inference of Population Structure from Multilocus Sequence Typing Data" (in en). Frontiers in Microbiology 7: 1599. 2016. doi:10.3389/fmicb.2016.01599. PMID 27803691. 
  3. ↑ "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. 2010. PMID 21038805. 
  4. ↑ "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. August 2016. doi:10.1016/j.diagmicrobio.2016.05.008. PMID 27241371. 
  5. ↑ 5.0 5.1 5.2 5.3 5.4 5.5 5.6 5.7 5.8 "New insights in Staphylococcus pseudintermedius pathogenicity: antibiotic-resistant biofilm formation by a human wound-associated strain". BMC Microbiology 15: 109. May 2015. doi:10.1186/s12866-015-0449-x. PMID 25994406. 
  6. ↑ 6.00 6.01 6.02 6.03 6.04 6.05 6.06 6.07 6.08 6.09 6.10 "Pathogenicity potential of Staphylococcus pseudintermedius strains isolated from canine carriers and from dogs with infection signs". Virulence 4 (3): 255–9. April 2013. doi:10.4161/viru.23526. PMID 23328490. 
  7. ↑ 7.0 7.1 7.2 7.3 7.4 7.5 7.6 7.7 7.8 "Staphylococcus, Micrococcus, and Other Catalase-Positive Cocci". Manual of Clinical Microbiology, 10th Edition. American Society of Microbiology. 2011-01-01. pp. 308–330. doi:10.1128/9781555816728.ch19. ISBN 978-1-55581-463-2. 
  8. ↑ 8.0 8.1 8.2 8.3 "Identification of Staphylococcus intermedius Group by MALDI-TOF MS". Systematic and Applied Microbiology 34 (1): 45–51. February 2011. doi:10.1016/j.syapm.2010.11.004. PMID 21300509. 
  9. ↑ 9.0 9.1 9.2 "Species differentiation within the Staphylococcus intermedius group using a refined MALDI-TOF MS database". Clinical Microbiology and Infection 20 (10): 1007–15. October 2014. doi:10.1111/1469-0691.12662. PMID 24807701. 
  10. ↑ "Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus in Workers in the Food Industry". Staphylococcus aureus. Elsevier. 2018. pp. 163–188. doi:10.1016/b978-0-12-809671-0.00009-7. ISBN 978-0-12-809671-0. 
  11. ↑ 11.0 11.1 "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. August 2011. doi:10.1016/j.mimet.2011.04.019. PMID 21586304. 
  12. ↑ 12.0 12.1 12.2 12.3 12.4 "Reclassification of phenotypically identified staphylococcus intermedius strains". Journal of Clinical Microbiology 45 (9): 2770–8. September 2007. doi:10.1128/JCM.00360-07. PMID 17596353. 
  13. ↑ 13.0 13.1 13.2 "What's happened to Staphylococcus intermedius? Taxonomic revision and emergence of multi-drug resistance". The Journal of Small Animal Practice 53 (3): 147–54. March 2012. doi:10.1111/j.1748-5827.2011.01165.x. PMID 22251285. http://researchonline.rvc.ac.uk/id/eprint/5764/. 
  14. ↑ 14.0 14.1 "Staphylococcus pseudintermedius sp. nov., a coagulase-positive species from animals". International Journal of Systematic and Evolutionary Microbiology 55 (Pt 4): 1569–1573. July 2005. doi:10.1099/ijs.0.63413-0. PMID 16014483. 
  15. ↑ "Staphylococcus pseudintermedius 16S rRNA gene, type strain LMG 22219T" (in en-US). 2005-08-15. http://www.ncbi.nlm.nih.gov/nuccore/AJ780976.1. 
  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" (in en). https://lpsn.dsmz.de/species/staphylococcus-pseudintermedius. 
  18. ↑ "Oxoid - Product Detail". http://www.oxoid.com/uk/blue/prod_detail/prod_detail.asp?pr=CM0145&org=153&c=uk&lang=en#:~:text=Description-,Staphylococcus%20Medium%20No.,mannitol%20fermentation,%20and%20gelatin%20liquefaction. 
  19. ↑ 19.00 19.01 19.02 19.03 19.04 19.05 19.06 19.07 19.08 19.09 19.10 19.11 19.12 19.13 19.14 19.15 19.16 19.17 19.18 19.19 19.20 19.21 19.22 19.23 "Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity". Veterinary Dermatology 23 (4): 253–66, e51–2. August 2012. doi:10.1111/j.1365-3164.2012.01046.x. PMID 22515504. 
  20. ↑ "Identifying Bacteria Through Look, Growth, Stain and Strain". 2020-02-07. https://asm.org/Articles/2020/February/Identifying-Bacteria-Through-Look,-Growth,-Stain. 
  21. ↑ "Characterization of coagulase-positive Staphylococcus intermedius and Staphylococcus aureus isolated from veterinary clinical specimens". Journal of Clinical Microbiology 18 (4): 789–92. October 1983. doi:10.1128/JCM.18.4.789-792.1983. PMID 6630462. 
  22. ↑ 22.0 22.1 "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. April 2015. doi:10.1007/s10096-014-2300-y. PMID 25532507. 
  23. ↑ "Combining MALDI-TOF and genomics in the study of methicillin resistant and multidrug resistant Staphylococcus pseudintermedius in New Zealand". Scientific Reports 9 (1): 1271. February 2019. doi:10.1038/s41598-018-37503-9. PMID 30718644. Bibcode: 2019NatSR...9.1271N. 
  24. ↑ "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. 2020-07-23. doi:10.3389/fvets.2020.00376. PMID 32793641. 
  25. ↑ "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. March 2016. doi:10.1128/JCM.02864-15. PMID 26607988. 
  26. ↑ "Vitek 2 Antimicrobial Susceptibility Testing". Biomedical Safety & Standards 49 (4): 28. 2019. doi:10.1097/01.bmsas.0000553632.43991.10. 
  27. ↑ "NCCLS guidelines: revised performance standards for antimicrobial disk susceptibility tests". Antimicrobic Newsletter 1 (8): 64–65. 1984. doi:10.1016/0738-1751(84)90027-3. 
  28. ↑ "Carriage of methicillin-resistant staphylococci by healthy companion animals in the US". Letters in Applied Microbiology 59 (1): 1–8. July 2014. doi:10.1111/lam.12254. PMID 24730724. 
  29. ↑ 29.0 29.1 29.2 29.3 "Exploring Staphylococcus pseudintermedius: an emerging zoonotic pathogen?". Future Microbiology 11 (11): 1371–1374. October 2016. doi:10.2217/fmb-2016-0137. PMID 27750440. 
  30. ↑ 30.0 30.1 30.2 "Identification and molecular epidemiology of methicillin resistant Staphylococcus pseudintermedius strains isolated from canine clinical samples in Argentina". BMC Veterinary Research 15 (1): 264. July 2019. doi:10.1186/s12917-019-1990-x. PMID 31351494. 
  31. ↑ "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. June 2016. doi:10.1093/jac/dkw029. PMID 26944924. 
  32. ↑ "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. August 2010. doi:10.1093/jac/dkq203. PMID 20534627. 
  33. ↑ 33.0 33.1 "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. February 2013. doi:10.1111/j.1365-3164.2012.01051.x. PMID 23331692. 
  34. ↑ "Heterogeneity of methicillin-sensitive Staphylococcus pseudintermedius strains isolated from diseased dogs". Polish Journal of Veterinary Sciences 14 (2): 283–4. 2011. doi:10.2478/v10181-011-0043-6. PMID 21721415. 
  35. ↑ "Clonal diversity and biofilm-forming ability of methicillin-resistant Staphylococcus pseudintermedius". The Journal of Antimicrobial Chemotherapy 67 (4): 841–8. April 2012. doi:10.1093/jac/dkr576. PMID 22258925. 
  36. ↑ 36.0 36.1 "Epidemiology, Clinical Characteristics, and Antimicrobial Susceptibility Profiles of Human Clinical Isolates of Staphylococcus intermedius Group". Journal of Clinical Microbiology 56 (3). March 2018. doi:10.1128/JCM.01788-17. PMID 29305548. 
  37. ↑ 37.0 37.1 "Are zoonotic Staphylococcus pseudintermedius strains a growing threat for humans?". Folia Microbiologica 63 (6): 743–747. November 2018. doi:10.1007/s12223-018-0615-2. PMID 29804274. 
  38. ↑ 38.0 38.1 "Canine superficial pyoderma and therapeutic considerations". The Canadian Veterinary Journal 57 (2): 204–6. February 2016. PMID 26834275. 
  39. ↑ 39.0 39.1 39.2 39.3 39.4 "The Staphylococcus intermedius group of bacterial pathogens: species re-classification, pathogenesis and the emergence of meticillin resistance". Veterinary Dermatology 20 (5–6): 490–5. October 2009. doi:10.1111/j.1365-3164.2009.00828.x. PMID 20178486. 
  40. ↑ 40.0 40.1 "Cluster of infections caused by methicillin-resistant Staphylococcus pseudintermedius in humans in a tertiary hospital". Journal of Clinical Microbiology 52 (8): 3118–20. August 2014. doi:10.1128/JCM.00703-14. PMID 24871217. 
  41. ↑ 41.0 41.1 41.2 41.3 "Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71". The Journal of Antimicrobial Chemotherapy 65 (9): 2047–8. September 2010. doi:10.1093/jac/dkq241. PMID 20601356. 
  42. ↑ 42.0 42.1 42.2 "Staphylococcal Infections - Infectious Diseases" (in en-US). https://www.merckmanuals.com/professional/infectious-diseases/gram-positive-cocci/staphylococcal-infections. 
  43. ↑ 43.0 43.1 "Carriage of methicillin-resistant Staphylococcus pseudintermedius in small animal veterinarians: indirect evidence of zoonotic transmission". Zoonoses and Public Health 58 (8): 533–9. December 2011. doi:10.1111/j.1863-2378.2011.01398.x. PMID 21824350. 

Further reading

External links

Wikidata ☰ Q16992700 entry



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