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Staphylococcus pseudintermedius: Is it a real threat to human health?

Open Access
|Dec 2021

References

  1. Kawamura Y., Hou X.G., Sultana F., Hirose K., Miyake M., Shu S.E., Ezaki T. (1998). Distribution of Staphylococcus species among human clinical specimens and emended description of Staphylococcus caprae. J. Clin. Microbiol., 36: 2038-2042.
  2. Bierowiec K., Korzeniowska-Kowal A., Wzorek A., Rypuła K., Gamian A. (2019). Prevalence of Staphylococcus species colonization in healthy and sick cats. Biomed. Res. Int., 2019: 4360525.
  3. Gandolfi-Decristophoris P., Regula G., Petrini O., Zinsstag J., Schelling E. (2013). Prevalence and risk factors for carriage of multi-drug resistant Staphylococci in healthy cats and dogs. J. Vet. Sci., 14: 449-456.
  4. Bean D.C., Wigmore S.M. (2016). Carriage rate and antibiotic susceptibility of coagulase-positive staphylococci isolated from healthy dogs in Victoria, Australia. Aust. Vet. J., 94: 456-460.
  5. Kizerwetter-Świda M., Chrobak-Chmiel D., Rzewuska M.: (2018). Problemy weterynaryjnej diagnostyki mikrobiologicznej dotyczącej zakażeń gronkowcowych. Życie Wet., 93: 373-376.
  6. Ma G.C., Worthing K.A., Gottlieb T., Ward M.P., Norris J.M. (2020). Molecular characterization of community-associated methicillin-resistant Staphylococcus aureus from pet dogs. Zoonoses Public Health, 67: 222-230.
  7. Ruzauskas M., Couto N., Kerziene S., Siugzdiniene R., Klimiene I., Virgailis M., Pomba C. (2015). Prevalence, species distribution and antimicrobial resistance patterns of methicillin-resistant staphylococci in Lithuanian pet animals. Acta Vet. Scand., 57: 27.
  8. van Duijkeren E., Catry B., Greko C., Moreno M.A., Pomba M.C., Pyörälä S., Ruzauskas M., Sanders P., Threlfall E.J., Torren-Edo J., et al. (2011). Review on methicillin-resistant Staphylococcus pseudintermedius. J. Antimicrob. Chemother., 66: 2705-2714.
  9. Chrobak D., Kizerwetter-Świda M., Rzewuska M., Binek M. (2013). Staphylococcus pseudintermedius – nowy, ale dobrze znany patogen. Życie Wet., 88: 625-628.
  10. Kmieciak W., Szewczyk E.M. (2018). Are zoonotic Staphylococcus pseudintermedius strains a growing threat for humans? Folia Microbiol., 63: 743-747.
  11. Kuan E.C., Yoon A.J., Vijayan T., Humphries R.M., Suh J.D. (2016). Canine Staphylococcus pseudintermedius sinonasal infection in human hosts. Int. Forum Allergy Rhinol., 6: 710-715.
  12. Robb A.R., Wright E.D., Foster A.M., Walker R., Malone C. (2017). Skin infection caused by a novel strain of Staphylococcus pseudintermedius in a Siberian husky dog owner. JMM Case Rep., 4: jmmcr005087.
  13. Somayaji R., Priyantha M.A., Rubin J.E., Church D. (2016). Human infections due to Staphylococcus pseudintermedius, an emerging zoonosis of canine origin: Report of 24 cases. Diagn. Microbiol. Infect. Dis., 85: 471-476.
  14. Lee J., Murray A., Bendall R., Gaze W., Zhang L., Vos M. (2015). Improved detection of Staphylococcus intermedius group in a routine diagnostic laboratory. J. Clin. Microbiol., 53: 961-963.
  15. Murray A.K., Lee J., Bendall R., Zhang L., Sunde M., Schau Slettemeås J., Gaze W., Page A.J., Vos M. (2018). Staphylococcus cornubiensis sp. nov., a member of the Staphylococcus intermedius Group (SIG). Int. J. Syst. Evol. Microbiol., 68: 3404-3408.
  16. Markey B., Leonard F., Archambault M., Cullinane A., Maguire D. (2013). Clinical veterinary microbiology. 2nd Edition. Maryland Heights, MO: Mosby.
  17. Devriese L.A., Vancanneyt M., Baele M., Vaneechoutte M., De Graef E., Snauwaert C., Cleenwerck I., Dawyndt P., Swings J., Decostere A., Haesebrouck F. (2005). Staphylococcus pseudintermedius sp. nov., a coagulase-positive species from animals. Int. J. Syst. Evol. Microbiol., 55: 1569-1573.
  18. Sasaki T., Kikuchi K., Tanaka Y., Takahashi N., Kamata S., Hiramatsu K. (2007). Reclassification of phenotypically identified Staphylococcus intermedius strains. J. Clin. Microbiol., 45: 2770-2778.
  19. Sasaki T., Kikuchi K., Tanaka Y., Takahashi N., Kamata S., Hiramatsu K. (2007). Methicillin-resistant Staphylococcus pseudintermedius in a veterinary teaching hospital. J. Clin. Microbiol., 45: 1118-1125.
  20. Bannoehr J., Franco A., Iurescia M., Battisti A., Fitzgerald J.R. (2009). Molecular diagnostic identification of Staphylococcus pseudintermedius. J. Clin. Microbiol., 47: 469-471.
  21. Sasaki T., Tsubakishita S., Tanaka Y., Sakusabe A., Ohtsuka M., Hirotaki S., Kawakami T., Fukata T., Hiramatsu K. (2010). Multiplex-PCR method for species identification of coagulase-positive staphylococci. J. Clin. Microbiol., 48: 765-769.
  22. Silva M.B., Ferreira F.A., Garcia L.N., Silva-Carvalho M.C., Botelho L.A., Figueiredo A.M., Vieira-da-Motta O. (2015). An evaluation of matrix-assisted laser desorption ionization time-of-flight mass spectrometry for the identification of Staphylococcus pseudintermedius isolates from canine infections. J. Vet. Diagn. Invest., 27: 231-235.
  23. Marszalik A., Chrobak-Chmiel D., Golke A., Sałamaszyńska-Guz A., Dembele K. (2018). Staphylococcus pseudintermedius – czy wiemy o nim wszystko? Życie Wet., 93: 238-240.
  24. Fitzgerald J.R. (2009). The Staphylococcus intermedius group of bacterial pathogens: Species re-classification, pathogenesis and the emergence of meticillin resistance. Vet. Dermatol., 20: 490-495.
  25. Maali Y., Badiou C., Martins-Simões P., Hodile E., Bes M., Vandenesch F., Lina G., Diot A., Laurent F., Trouillet-Assant S. (2018). Understanding the virulence of Staphylococcus pseudintermedius A major role of pore-forming toxins. Front. Cell. Infect. Microbiol., 8: 221.
  26. Crawford E.C., Singh A., Gibson T.W., Scott Weese J. (2016). Biofilm-associated gene expression in Staphylococcus pseudintermedius on a variety of implant materials. Vet. Surg., 45: 499-506.
  27. Casagrande Proietti P., Stefanetti V., Hyatt D.R., Marenzoni M.L., Capomaccio S., Coletti M., Bietta A., Franciosini M.P., Passamonti F. (2015). Phenotypic and genotypic characterization of canine pyoderma isolates of Staphylococcus pseudintermedius for biofilm formation. J. Vet. Med. Sci., 77: 945-951.
  28. O’Gara J.P. (2007). Ica and beyond: Biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett., 270: 179-188.
  29. Czyżewska-Dors E., Dors A., Pomorska-Mól M. (2018). Właściwości biofilmu bakteryjnego warunkujące oporność na antybiotyki oraz metody jego zwalczania. Życie Wet., 93: 765-771.
  30. Chan W.Y., Hickey E.E., Page S.W., Trott D.J., Hill P.B. (2019). Biofilm production by pathogens associated with canine otitis externa, and the antibiofilm activity of ionophores and antimicrobial adjuvants. J. Vet. Pharmacol. Ther., 42: 682-692.
  31. Meroni G., Soares Filipe J.F., Drago L., Martino P.A. (2019). Investigation on antibiotic-resistance, biofilm formation and virulence factors in multi drug resistant and non multi drug resistant Staphylococcus pseudintermedius. Microorganisms, 7: 702.
  32. Paul N.C. (2015). MRSP: Prevalence in practice. Vet. Rec., 176: 170-171.
  33. Stefanetti V., Bietta A., Pascucci L., Marenzoni M.L., Coletti M., Franciosini M.P., Passamonti F., Proietti P.C. (2017). Investigation of the antibiotic resistance and biofilm formation of Staphylococcus pseudintermedius strains isolated from canine pyoderma. Vet. Ital., 53: 289-296.
  34. Grönthal T., Eklund M., Thomson K., Piiparinen H., Sironen T., Rantala M. (2017). Antimicrobial resistance in Staphylococcus pseudintermedius and the molecular epidemiology of methicillin-resistant S. pseudintermedius in small animals in Finland. J. Anti-microb. Chemother., 72: 1021-1030.
  35. Rodrigues A.C., Belas A., Marques C., Cruz L., Gama L.T., Pomba C. (2018). Risk factors for nasal colonization by methicillin-resistant staphylococci in healthy humans in professional daily contact with companion animals in Portugal. Microb. Drug. Resist., 24: 434-446.
  36. Wegener A., Damborg P., Guardabassi L., Moodley A., Mughini-Gras L., Duim B., Wagenaar J.A., Broens E.M. (2020). Specific staphylococcal cassette chromosome mec (SCCmec types and clonal complexes are associated with low-level amoxicillin/clavulanic acid and cefalotin resistance in methicillin-resistant Staphylococcus pseudintermedius. J. Antimicrob. Chemother., 75: 508-511.
  37. Worthing K.A., Brown J., Gerber L., Trott D.J., Abraham S., Norris J.M. (2018). Methicillin-resistant staphylococci amongst veterinary personnel, personnel-owned pets, patients and the hospital environment of two small animal veterinary hospitals. Vet. Microbiol., 223: 79-85.
  38. Duim B., Verstappen K.M., Kalupahana R.S., Ranathunga L., Fluit A.C., Wagenaar J.A. (2018). Methicillin-resistant Staphylococcus pseudintermedius among dogs in the description of novel SCCmec variants. Vet. Microbiol., 213: 136-141.
  39. International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009). Classification of staphylococcal cassette chromosome mec (SCCmec Guidelines for reporting novel SCCmec elements. Antimicrob. Agents Chemother., 53: 4961-4967.
  40. Krapf M., Müller E., Reissig A., Slickers P., Braun S.D., Müller E., Ehricht R., Monecke S. (2019). Molecular characterisation of methicillin-resistant Staphylococcus pseudintermedius from dogs and the description of their SCCmec elements. Vet. Microbiol., 233: 196-203.
  41. Worthing K.A., Schwendener S., Perreten V., Saputra S., Coombs G.W., Pang S., Davies M.R., Abraham S., Trott D.J., Norris J.M. (2018). Characterization of staphylococcal cassette chromosome mec elements from methicillin-resistant Staphylococcus pseudintermedius infections in Australian animals. mSphere, 3: e00491-18.
  42. Hartmann F.A., White D.G., West S.E., Walker R.D., Deboer D.J. (2005). Molecular characterization of Staphylococcus intermedius carriage by healthy dogs and comparison of antimicrobial susceptibility patterns to isolates from dogs with pyoderma. Vet. Microbiol., 108: 119-131.
  43. Tanner M.A., Everett C.L., Youvan D.C. (2000). Molecular phylogenetic evidence for noninvasive zoonotic transmission of Staphylococcus intermedius from a canine pet to a human. J. Clin. Microbiol., 38: 1628-1631.
  44. Griffeth G.C., Morris D.O., Abraham J.L., Shofer F.S., Rankin S.C. (2008). Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Vet. Dermatol., 19: 142-149.
  45. Han J.I., Rhim H., Yang C.H., Park H.M. (2018). Molecular characteristics of new clonal complexes of Staphylococcus pseudintermedius from clinically normal dogs. Vet. Q., 38: 14-20.
  46. Hanselman B.A., Kruth S.A., Rousseau J., Weese J.S. (2009). Coagulase positive staphylococcal colonization of humans and their household pets. Can. Vet. J., 50: 954-958.
  47. Lee C.H., Park Y.K., Shin S., Park Y.H., Park K.T. (2018). Characterization of methicillin-resistant Staphylococcus pseudintermedius isolated from dogs in veterinary hospitals in Korea. Intern. J. Appl. Res. Vet. Med., 16: 211-220.
  48. Rubin J.E., Chirino-Trejo M. (2011). Prevalence, sites of colonization, and antimicrobial resistance among Staphylococcus pseudintermedius isolated from healthy dogs in Saskatoon, Canada. J. Vet. Diagn. Invest., 23: 351-354.
  49. Feng Y., Tian W., Lin D. Luo Q., Zhou Y., Yang T., Deng Y., Liu Y.H., Liu J.H. (2012). Prevalence and characterization of methicillin-resistant Staphylococcus pseudintermedius in pets from South China. Vet. Microbiol., 160: 517-524.
  50. Kalhoro D.H., Kalhoro M.S., Mangi M.H., Jahejo A.R., Kumbhar S., Lochi G.M., Mari G.M., Kaka A., Lund A.K., Liu Y.J. (2019). Antimicrobial resistance of staphylococci and streptococci isolated from dogs. Trop. Biomed, 36: 468-474.
  51. Maluping R.P., Paul N.C., Moodley A. (2014). Antimicrobial susceptibility of methicillin-resistant Staphylococcus pseudintermedius isolated from veterinary clinical cases in the UK. Br. J. Biomed. Sci., 71: 55-57.
  52. Marques C., Belas A., Franco A., Aboim C., Gama L.T., Pomba C. (2018). Increase in antimicrobial resistance and emergence of major international high-risk clonal lineages in dogs and cats with urinary tract infection: 16 year retrospective study. J. Antimicrob. Chemother., 73: 377-384.
  53. Fazakerley J., Nuttall T., Sales D., Schmidt V., Carter S.D., Hart C.A., McEwan N.A. (2009). Staphylococcal colonization of mucosal and lesional skin sites in atopic and healthy dogs. Vet. Dermatol., 20: 179-184.
  54. Furiani N., Scarampella F., Martino P.A., Panzini I., Fabbri E., Ordeix L. (2011). Evaluation of the bacterial microflora of the conjunctival sac of healthy dogs and dogs with atopic dermatitis. Vet. Dermatol., 22: 490-496.
  55. Corrò M., Skarin J., Börjesson S., Rota A. (2018). Occurrence and characterization of methicillin-resistant Staphylococcus pseudintermedius in successive parturitions of bitches and their puppies in two kennels in Italy. BMC Vet. Res., 14: 308.
  56. Zakošek Pipan M., Švara T., Zdovc I., Papić B., Avberšek J., Kušar D., Mrkun J. (2019). Staphylococcus pseudintermedius septicemia in puppies after elective cesarean section: Confirmed transmission via dam’s milk. BMC Vet. Res., 15: 41.
  57. Qekwana D.N., Sebola D., Oguttu J.W., Odoi A. (2017). Antimicrobial resistance patterns of Staphylococcus species isolated from cats presented at a veterinary academic hospital in South Africa. BMC Vet. Res., 13: 286.
  58. Wettstein K., Descloux S., Rossano A., Perreten V. (2008). Emergence of methicillin-resistant Staphylococcus pseudintermedius in Switzerland: Three cases of urinary tract infections in cats. Schweiz Arch. Tierheilkd., 150: 339-343.
  59. Lehner G., Linek M., Bond R., Lloyd D.H., Prenger-Berninghoff E., Thom N., Straube I., Verheyen K., Loeffler A. (2014). Case-control risk factor study of methicillin-resistant Staphylococcus pseudintermedius (MRSP) infection in dogs and cats in Germany. Vet. Microbiol., 168: 154-160.
  60. Espadale E., Pinchbeck G., Williams N.J., Timofte D., McIntyre K.M., Schmidt V.M. (2018). Are the hands of veterinary staff a reservoir for antimicrobial-resistant bacteria? A randomized study to evaluate two hand hygiene rubs in a veterinary hospital. Microb. Drug Resist., 24: 1607-1616
  61. Feßler A.T., Schuenemann R., Kadlec K. Hensel V., Brombach J., Murugaiyan J., Oechtering G., Burgener I.A., Schwarz S. (2018). Methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus pseudintermedius (MRSP) among employees and in the environment of a small animal hospital. Vet. Microbiol., 221: 153-158.
  62. Youn J.H., Park Y.H., Hang’ombe B., Sugimoto C. (2014). Prevalence and characterization of Staphylococcus aureus and Staphylococcus pseudintermedius isolated from companion animals and environment in the veterinary teaching hospital in Zambia, Africa. Comp. Immunol. Microbiol. Infect. Dis., 37: 123-130.
  63. Van Hoovels L., Vankeerberghen A., Boel A., Van Vaerenbergh K., De Beenhouwer H. (2006). First case of Staphylococcus pseudintermedius infection in a human. J. Clin. Microbiol., 44: 4609-4612.
  64. Ference E.H., Danielian A., Kim H.W., Yoo F., Kuan E.C., Suh J.D. (2019). Zoonotic Staphylococcus pseudintermedius sinonasal infections: Risk factors and resistance patterns. Int. Forum Allergy Rhinol., 9: 724-729.
  65. Paul N.C., Moodley A., Ghibaudo G., Guardabassi L. (2011). Carriage of methicillin-resistant Staphylococcus pseudintermedius in small animal veterinarians: Indirect evidence of zoonotic transmission. Zoonoses Public Health, 58: 533-539.
  66. Somayaji R., Rubin J.E., Priyantha M.A., Church D. (2016). Exploring Staphylococcus pseudintermedius An emerging zoonotic pathogen? Future Microbiol., 11: 1371-1374
  67. Gagetti P., Errecalde L., Wattam A.R., De Belder D., Ojeda Saavedra M., Corso A., Rosato A.E. (2020). Characterization of the first mecA-positive multidrug-resistant Staphylococcus pseudintermedius isolated from an Argentinian patient. Microb. Drug Resist., 26: 717-721.
  68. Börjesson S., Gómez-Sanz E., Ekström K., Torres C., Grönlund U. (2015). Staphylococcus pseudintermedius can be misdiagnosed as Staphylococcus aureus in humans with dog bite wounds. Eur. J. Clin. Microbiol. Infect. Dis., 34: 839-844.
  69. Darlow C.A., Paidakakos N., Sikander M., Atkins B. (2017). A spinal infection with Staphylococcus pseudintermedius. BMJ Case Rep., 2017: bcr2017221260
  70. Diaz M.A., Gardner L.B., Libertin C.R. (2019). Staphylococcus pseudintermedius catheter-related bloodstream infection after exposure to domestic dogs and a cat. BMJ Case Rep., 12: e231489.
  71. Lozano C., Rezusta A., Ferrer I., Pérez-Laguna V., Zarazaga M., Ruiz-Ripa L., Revillo M.J., Torres C. (2017). Staphylococcus pseudintermedius human infection cases in Spain: Dog-to-human transmission. Vector Borne Zoonotic Dis., 17: 268-270.
  72. Pompilio A., De Nicola S., Crocetta V., Guarnieri S., Savini V., Carretto E., Di Bonaventura G. (2015). New insights in Staphylococcus pseudintermedius pathogenicity: Antibiotic-resistant biofilm formation by a human wound-associated strain. BMC Microbiol., 15: 109.
Language: English
Page range: 980 - 986
Submitted on: Sep 23, 2020
Accepted on: Jul 13, 2021
Published on: Dec 29, 2021
Published by: Hirszfeld Institute of Immunology and Experimental Therapy
In partnership with: Paradigm Publishing Services
Publication frequency: 1 issue per year

© 2021 Marta Miszczak, Sonia Lachowska, Karolina Bierowiec, published by Hirszfeld Institute of Immunology and Experimental Therapy
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