Characterisation of methicillin-susceptible Staphylococcus pseudintermedius isolates from canine infections and determination of virulence factors using multiplex PCR O., Svec P., Tkadlec J., Doskar J., Kinska H., Pantucek R. (2017): Characterisation of methicillin-susceptible Staphylococcus pseudintermedius isolates from canine infections and determination of virulence factors using multiplex PCR. Veterinarni Medicina, 62: 81-89.
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Staphylococcus pseudintermedius is a genuine opportunistic pathogen of the skin, especially in canids. However, characterisation of virulence, antimicrobial resistance and genotypic variability in methicillin-susceptible S. pseudintermedius isolates has not been fully explored. In this study, coagulase-positive staphylococcal isolates collected from dogs of various breeds and ages suffering from dermatitis (n = 70), pyoderma (n = 7), and otitis (n = 7), from districts of Prague (Czech Republic) and surrounding areas, were characterised using matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry, and repetitive sequence-based PCR fingerprinting. Susceptibility to antimicrobial agents was determined, virulence factor genes for leukocidin (lukSF-I), exfoliatins (exi, expB, and siet), enterotoxin C (seccanine) and enterotoxin-related genes (se-int and sel) were detected using multiplex PCR and the genotypes of S. pseudintermedius isolates were determined using SmaI macrorestriction analysis. The majority of the staphylococcal isolates (n = 84) were identified as S. pseudintermedius (n = 79) and all of them were susceptible to methicillin/oxacillin (MSSP). About half of the strains (n = 41) were resistant to macrolide-lincosamide-streptogramin B antimicrobial agents and resistance was mediated in all but one of the strains by the erm(B) gene. The genes for lukSF-I, siet, se-int, and sel were detected in the majority of the MSSP strains (96.2%, 100%, 100%, and 73.4%, respectively). Investigated canine S. pseudintermedius isolates were highly heterogeneous, which prevented the correlation of any specific lineage to a particular infection, dog breed, or region of origin.
Bannoehr Jeanette, Guardabassi Luca (2012): Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity. Veterinary Dermatology, 23, 253-e52
Bannoehr J., Ben Zakour N. L., Waller A. S., Guardabassi L., Thoday K. L., van den Broek A. H. M., Fitzgerald J. R. (): Population Genetic Structure of the Staphylococcus intermedius Group: Insights into agr Diversification and the Emergence of Methicillin-Resistant Strains. Journal of Bacteriology, 189, 8685-8692
BARON FLORENCE, COCHET MARIE-FRANÇOISE, PELLERIN JEAN-LOUIS, BEN ZAKOUR NOURI, LEBON ANNE, NAVARRO ANNE, PROUDY ISABELLE, LE LOIR YVES, GAUTIER MICHEL (2004): Development of a PCR Test To Differentiate between Staphylococcus aureus and Staphylococcus intermedius. Journal of Food Protection, 67, 2302-2305
Becker K., Keller B., von Eiff C., Bruck M., Lubritz G., Etienne J., Peters G. (2001): Enterotoxigenic Potential of Staphylococcus intermedius. Applied and Environmental Microbiology, 67, 5551-5557
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. European Journal of Clinical Microbiology & Infectious Diseases, 34, 839-844
Chanchaithong Pattrarat, Prapasarakul Nuvee (2011): Biochemical markers and protein pattern analysis for canine coagulase-positive staphylococci and their distribution on dog skin. Journal of Microbiological Methods, 86, 175-181
Couto Natacha, Belas Adriana, Couto Isabel, Perreten Vincent, Pomba Constança (2014): Genetic Relatedness, Antimicrobial and Biocide Susceptibility Comparative Analysis of Methicillin-Resistant and -Susceptible Staphylococcus pseudintermedius from Portugal. Microbial Drug Resistance, 20, 364-371
Decristophoris Paola, Fasola Amy, Benagli Cinzia, Tonolla Mauro, Petrini Orlando (2011): Identification of Staphylococcus intermedius Group by MALDI-TOF MS. Systematic and Applied Microbiology, 34, 45-51
Fazakerley Jennifer, Williams Nicola, Carter Stuart, McEwan Neil, Nuttall Tim (2010): Heterogeneity of Staphylococcus pseudintermedius isolates from atopic and healthy dogs. Veterinary Dermatology, 21, 578-585
Futagawa-Saito K., Suzuki M., Ohsawa M., Ohshima S., Sakurai N., Ba-Thein W., Fukuyasu T. (2004): Identification and prevalence of an enterotoxin-related gene, se-int, in Staphylococcus intermedius isolates from dogs and pigeons. Journal of Applied Microbiology, 96, 1361-1366
Futagawa-Saito Keiko, Makino Shinichiroh, Sunaga Fujiko, Kato Yukio, Sakurai-Komada Naomi, Ba-Thein William, Fukuyasu Tsuguaki (2009): Identification of first exfoliative toxin in Staphylococcus pseudintermedius. FEMS Microbiology Letters, 301, 176-180
Garbacz K., Piechowicz L., Żarnowska S., Haras K., Dąbrowska-Szponar M. (2011): Heterogeneity of methicillin-sensitive Staphylococcus pseudintermedius strains isolated from diseased dogs. Polish Journal of Veterinary Sciences, 14, -
Gómez-Sanz Elena, Torres Carmen, Lozano Carmen, Zarazaga Myriam (2013): High diversity of Staphylococcus aureus and Staphylococcus pseudintermedius lineages and toxigenic traits in healthy pet-owning household members. Underestimating normal household contact?. Comparative Immunology, Microbiology and Infectious Diseases, 36, 83-94
Haenni Marisa, de Moraes Natasha Alves, Châtre Pierre, Médaille Christine, Moodley Arshnee, Madec Jean-Yves (2014): Characterisation of clinical canine meticillin-resistant and meticillin-susceptible Staphylococcus pseudintermedius in France. Journal of Global Antimicrobial Resistance, 2, 119-123
Hendricks Anke, Schuberth Hans-Joachim, Schueler Karen, Lloyd David H (2002): Frequency of superantigen-producing Staphylococcus intermedius isolates from canine pyoderma and proliferation-inducing potential of superantigens in dogs. Research in Veterinary Science, 73, 273-277
Hesselbarth J., Witte W., Cuny C., Rohde R., Amtsberg G. (1994): Characterization of Staphylococcus intermedius from healthy dogs and cases of superficial pyoderma by DNA restriction endonuclease patterns. Veterinary Microbiology, 41, 259-266
Iyori Keita, Hisatsune Junzo, Kawakami Tetsuji, Shibata Sanae, Murayama Nobuo, Ide Kaori, Nagata Masahiko, Fukata Tsuneo, Iwasaki Toshiroh, Oshima Kenshiro, Hattori Masahira, Sugai Motoyuki, Nishifuji Koji (2010): Identification of a novel Staphylococcus pseudintermedius exfoliative toxin gene and its prevalence in isolates from canines with pyoderma and healthy dogs. FEMS Microbiology Letters, 312, 169-175
Kadlec Kristina, Schwarz Stefan (2012): Antimicrobial resistance of Staphylococcus pseudintermedius. Veterinary Dermatology, 23, 276-e55
KAWAKAMI Tetsuji, SHIBATA Sanae, MURAYAMA Nobuo, NAGATA Masahiko, NISHIFUJI Koji, IWASAKI Toshiroh, FUKATA Tsuneo (2010): Antimicrobial Susceptibility and Methicillin Resistance in Staphylococcus pseudintermedius and Staphylococcus schleiferi subsp. coagulans Isolated from Dogs with Pyoderma in Japan. Journal of Veterinary Medical Science, 72, 1615-1619
Lautz S., Kanbar T., Alber J., Lämmler C., Weiss R., Prenger-Berninghoff E., Zschöck M. (2006): Dissemination of the Gene Encoding Exfoliative Toxin of Staphylococcus intermedius Among Strains Isolated from Dogs During Routine Microbiological Diagnostics. Journal of Veterinary Medicine Series B, 53, 434-438
Lina G, Quaglia A, Reverdy ME, Leclercq R, Vandenesch F, Etienne J (1999): Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci. Antimicrobial Agents and Chemotherapy 43, 1062–1066.
Loeffler Anette, Linek Monika, Moodley Arshnee, Guardabassi Luca, Sung Julia M. L., Winkler Margit, Weiss Reinhard, Lloyd David H. (2007): First report of multiresistant, mecA-positive Staphylococcus intermedius in Europe: 12 cases from a veterinary dermatology referral clinic in Germany. Veterinary Dermatology, 18, 412-421
Moodley A, Riley MC, Kania SA, Guardabassi L (2013): Genome sequence of Staphylococcus pseudintermedius strain E140, an ST71 European-associated methicillin-resistant isolate. Genome Announcements 1. Available at
Norström Madelaine, Sunde Marianne, Tharaldsen Hanne, Mørk Tormod, Bergsjø Bjarne, Kruse Hilde (2009): Antimicrobial Resistance in Staphylococcus pseudintermedius in the Norwegian Dog Population. Microbial Drug Resistance, 15, 55-59
Onuma Kenta, Tanabe Taishi, Sato Hisaaki (2012): Antimicrobial resistance of Staphylococcus pseudintermedius isolates from healthy dogs and dogs affected with pyoderma in Japan. Veterinary Dermatology, 23, 17-e5
Paul Narayan Chandra, Bärgman Sofia Cathrine, Moodley Arshnee, Nielsen Søren Saxmose, Guardabassi Luca (2012): Staphylococcus pseudintermedius colonization patterns and strain diversity in healthy dogs: A cross-sectional and longitudinal study. Veterinary Microbiology, 160, 420-427
Perreten V., Kadlec K., Schwarz S., Gronlund Andersson U., Finn M., Greko C., Moodley A., Kania S. A., Frank L. A., Bemis D. A., Franco A., Iurescia M., Battisti A., Duim B., Wagenaar J. A., van Duijkeren E., Weese J. S., Fitzgerald J. R., Rossano A., Guardabassi L. (): Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. Journal of Antimicrobial Chemotherapy, 65, 1145-1154
Ruscher Claudia, Lübke-Becker Antina, Wleklinski Claus-G., Şoba Alexandra, Wieler Lothar H., Walther Birgit (2009): Prevalence of Methicillin-resistant Staphylococcus pseudintermedius isolated from clinical samples of companion animals and equidaes. Veterinary Microbiology, 136, 197-201
Ruscher Claudia, Lübke-Becker Antina, Semmler Torsten, Wleklinski Claus-G., Paasch Angela, Šoba Alexandra, Stamm Ivonne, Kopp Peter, Wieler Lothar H., Walther Birgit (2010): Widespread rapid emergence of a distinct methicillin- and multidrug-resistant Staphylococcus pseudintermedius (MRSP) genetic lineage in Europe. Veterinary Microbiology, 144, 340-346
SASAKI Asako, SHIMIZU Akira, KAWANO Junichi, WAKITA Yoshihisa, HAYASHI Toshikatsu, OOTSUKI Shigenobu (2005): Characteristics of Staphylococcus intermedius Isolates from Diseased and Healthy Dogs. Journal of Veterinary Medical Science, 67, 103-106
Schwarz S., Kadlec K., Strommenger B. (2007): Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius detected in the BfT-GermVet monitoring programme 2004-2006 in Germany. Journal of Antimicrobial Chemotherapy, 61, 282-285
Slettemeas J. S., Mikalsen J., Sunde M. (2010): Further Diversity of the Staphylococcus Intermedius Group and Heterogeneity in the MboI Restriction Site Used for Staphylococcus Pseudintermedius Species Identification. Journal of Veterinary Diagnostic Investigation, 22, 756-759
Solyman S. M., Black C. C., Duim B., Perreten V., van Duijkeren E., Wagenaar J. A., Eberlein L. C., Sadeghi L. N., Videla R., Bemis D. A., Kania S. A. (): Multilocus Sequence Typing for Characterization of Staphylococcus pseudintermedius. Journal of Clinical Microbiology, 51, 306-310
Štěpán J., Pantůček R., Růžičková V., Rosypal S., Hájek V., Doškař J. (2001): Identification of Staphylococcus aureus based on PCR amplification of species specific genomic 826 bp sequence derived from a common 44-kb Sma I restriction fragment. Molecular and Cellular Probes, 15, 249-257
Švec Pavel, Pantůček Roman, Petráš Petr, Sedláček Ivo, Nováková Dana (2010): Identification of Staphylococcus spp. using (GTG)5-PCR fingerprinting. Systematic and Applied Microbiology, 33, 451-456
Tanabe T, Toyoguchi M, Hirano F, Chiba M, Onuma K, Sato H (2013): Prevalence of staphylococcal enterotoxins in Staphylococcus pseudintermedius isolates from dogs with pyoderma and healthy dogs. Microbiology and Immunology 57, 651–654.
Weese J. S. (): Phenotypic Identification of Staphylococcus intermedius May Be Inaccurate. Journal of Clinical Microbiology, 51, 734-734
Yoon Jang W., Lee Gi-Jong, Lee So-Young, Park Chul, Yoo Jong-Hyun, Park Hee-Myung (2010): Prevalence of genes for enterotoxins, toxic shock syndrome toxin 1 and exfoliative toxin among clinical isolates of Staphylococcus pseudintermedius from canine origin. Veterinary Dermatology, 21, 484-489
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