期刊论文详细信息
BMC Microbiology
Variability of antibiotic susceptibility and toxin production of Staphylococcus aureus strains isolated from skin, soft tissue, and bone related infections
Lamine Baba-Moussa7  Gilles Prévost3  Simeon O Kotchoni2  Ymkje Stienstra1  Yves Barogui6  Honoré S Bankolé4  Daniel Keller3  Wardi Moussaoui3  Théodora A Ahoyo5  Haziz Sina7 
[1]Department of Internal Medicine/Infectious Diseases, University of Groningen, University Medical Center Groningen, P.O. Box 30.001, Groningen 9700 RB, The Netherlands
[2]Department of Biology and Center for Computational and Integrative Biology, Rutgers University, Camden NJ 08102, USA
[3]Unité: EA-4438 Physiopathologie et Médecine, Institut de Bactériologie, 3 rue Koeberlé, Strasbourg F-67000, France
[4]Laboratoire National de Santé Publique, Cotonou, Bénin
[5]EPAC/ Université d’Abomey-Calavi, Cotonou 01 BP 526, BENIN
[6]Programme National de Lutte contre l'Ulcère de Buruli, Cotonou, Benin
[7]Laboratoire de Biologie et de Typage Moléculaire en Microbiologie
[8] Faculté des Sciences et Techniques/Université d’Abomey-Calavi, Cotonou 05 BP 1604, BENIN
关键词: Africa;    Benin;    Skin infections;    Osteomyelitis;    Pyomyositis;    PVL;    MRSA;    S. aureus;   
Others  :  1143273
DOI  :  10.1186/1471-2180-13-188
 received in 2013-03-20, accepted in 2013-08-07,  发布年份 2013
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【 摘 要 】

Background

Staphylococcus aureus is an opportunistic commensal bacterium that mostly colonizes the skin and soft tissues. The pathogenicity of S. aureus is due to both its ability to resist antibiotics, and the production of toxins. Here, we characterize a group of genes responsible for toxin production and antibiotic resistance of S. aureus strains isolated from skin, soft tissue, and bone related infections.

Results

A total of 136 S. aureus strains were collected from five different types of infection: furuncles, pyomyositis, abscesses, Buruli ulcers, and osteomyelitis, from hospital admissions and out-patients in Benin. All strains were resistant to benzyl penicillin, while 25% were resistant to methicillin, and all showed sensitivity to vancomycin. Panton-Valentine leukocidin (PVL) was the most commonly produced virulence factor (70%), followed by staphylococcal enterotoxin B (44%). Exfoliative toxin B was produced by 1.3% of the strains, and was only found in isolates from Buruli ulcers. The tsst-1, sec, and seh genes were rarely detected (≤1%).

Conclusions

This study provides new insight into the prevalence of toxin and antibiotic resistance genes in S. aureus strains responsible for skin, soft tissue, and bone infections. Our results showed that PVL was strongly associated with pyomyositis and osteomyelitis, and that there is a high prevalence of PVL-MRSA skin infections in Benin.

【 授权许可】

   
2013 Sina et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Kluytmans A, van Belkum A, Verbrugh H: Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbial Rev 1997, 10(3):505-520.
  • [2]Nubel U, Roumagnac P, Feldkamp M, Song JH, Ko KS, Huang YC, Coombs G, Ip M, Westh H, Skov R, Struelens MJ, Goering RV, Strommenger B, Weller A, Witte W, Achtman M: Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 2008, 105:14130-14135.
  • [3]Holmes A, Ganner M, McGuane S, Pitt TL, Cookson BD, Kearns AM: Staphylococcus aureus Isolates Carrying Panton-Valentine Genes in England and Wales: Frequency, Characterization, and Association with Clinical Desease. J Clin Microbiol 2005, 43(5):2384-2390.
  • [4]Baba-Moussa L, Anani L, Scheftel JM, Couturier M, Riegel P, Haikou N, Hounsou F, Monteil H, Sanni A, Prevost G: Virulence factors produced by strains of Staphylococcus aureus isolated from urinary tract infections. J Hosp Infect 2008, 68:32-38.
  • [5]Baba-Moussa L, Ahissou H, Azokpota P, Assogba B, Atindéhou M, Anagonou S, Keller D, Sanni A, Prévost G: Toxins and adhesion factors associated with Staphylococcus aureus strains isolated from diarrheal patients in Benin. Afr J Biotechnol 2010, 9:604-611.
  • [6]Bohach GA, Fast DJ, Nelson RD, Schlievert PM: Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses. Crit Rev Microbiol 1990, 17:251-272.
  • [7]Breneman DL: Bacterial infection of the skin and soft tissues and their treatment. Curr Opin Infect Dis 1993, 6:678-682.
  • [8]Murray DL, Ohlendorf DH, Schlievert PM: Staphylococcal and streptococcal superantigens: their role in human diseases. ASM News 1995, 61:229-235.
  • [9]Dinges MM, Orwin PM, Schlievert PM: Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 2000, 13:16-34.
  • [10]Barg NL, Harris T: Toxin-mediated syndromes. In The staphylococci in human disease. Edited by Crossley KB, Archer GL. New York: Churchill Livingstone; 1997:527-544.
  • [11]Durupt F, Mayor L, Bes M, Reverdy ME, Vandenesch F, Thomas L, Etienne J: Prevalence of Staphylococcus aureus toxins and nasal carriage in furuncles and impetigo. Br J Dermatol 2007, 157:1161-1167.
  • [12]Gladstone GP, Van Heyningen WE: Staphylococcal leucocidins. Br J Exp Pathol 1957, 38:123-137.
  • [13]Woodin AM: Fractionation of a leucocidin from Staphylococcus aureus. Bioch J 1959, 73:225-237.
  • [14]Szmigielski S, Sobiczewska E, Prévost G, Monteil H, Colin DA, Jeljaszewicz J: Effect of purified staphylococcal leukocidal toxins on isolated blood polymorphonuclear leukocytes and peritoneal macrophages in vitro. Zentralbl Bakteriol 1998, 288:383-394.
  • [15]Hongo I, Baba T, Oishi K, Morimoto Y, Ito T, Hiramatsu K: Phenol-soluble modulin alpha 3 enhances the human neutrophil lysis mediated by Panton- Valentine leukocidin. J Infec Dis 2009, 200:715-723.
  • [16]Cribier B, Prevost G, Couppie P, Finck-Barbancon V, Grosshans E, Piemont Y: Staphylococcus aureus leukocidin: a new virulence factor in cutaneous infections? An epidemiological and experimental study. Dermatology 1992, 185:175-180.
  • [17]Couppié P, Cribier B, Prévost G, Grosshans E, Piémont Y: Leucocidin from Staphylococcus aureus and cutaneous infections: an epidemiological study. Arch Dermatol 1994, 130:1208-1209.
  • [18]Prevost G, Cribier B, Couppie P, Petiau P, Supersac G, Finck-Barbancon V, Monteil H, Piemont Y: Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect Immun 1995, 63:4121-4129.
  • [19]Lina G, Piémont Y, Godail-Gamot F, Bès M, Peter MO, Gauduchon V, Vandenesh F, Etienne J: Involvement of Panton Valentine leukocidineproducing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999, 29:1128-1132.
  • [20]Baba-Moussa L, Sina H, Scheftel JM, Moreau B, Sainte-Marie D, Kotchoni SO, Prevost G, Couppie P: Staphylococcal Panton-Valentine leucocidin as a major virulence factor associated to furuncles. PLoS One 2011, 6:e25716.
  • [21]Couppié P, Hommel D, Prévost G, Godart MC, Moreau B, Sainte- Marie D, Peneau C, Hulin A, Monteil H, Pradinaud R: Septicémie à Staphylococcus aureus, furoncle et leucocidine de Panton et Valentine: 3 observations. Ann Dermatol Venereol 1997, 124:684-686.
  • [22]Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, Vandenesch F, Piémont Y, Brousse N, Floret D, Etienne J: Association between Staphylococcus aureus strains carrying gene for Panton Valentin leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 2002, 359:753-759.
  • [23]Labandeira-Rey M, Couzon F, Boisset S, Brown EL, Bes M, Benito Y, Barbu EM, Vazquez V, Höök M, Etienne J, Vandenesch F, Bowden MG: Staphylococcus aureus Panton Valentine leukocidin causes necrotizing pneumonia. Science 2007, 315(5815):1130-1133.
  • [24]Diep BA, Palazzolo-Ballance AM, Tattevin P, Basuino L, Braughton KR, Whitney AR, Chen L, Kreiswirth BN, Otto M, DeLeo FR, Chambers HF: Contribution of Panton Valentine leukocidin in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. PLos One 2008, 3:e3198.
  • [25]Gillet Y, Dohin B, Dumitrescu O, Lina G, Vandenesch F, Etienne J, Floret D: Osteoarticular infections with Staphylococcus aureus secreting Panton Valentine leucocidin. Arch Pediatr 2007, 14(Suppl 2):102-107.
  • [26]Hussain A, Robinson GO, Malkin J, Duthie M, Kearns A, Perera N: Purpura fulminans in a child secondary to Panton Valentine leukocidinproducing Staphylococcus aureus. J Med Microbiol 2007, 56:1407-1409.
  • [27]Shivashankar GH, Murukesh N, Varma MP, Sharif IM, Glynn G: Infection by Panton Valentine leukocidin-producing Staphylococcus aureus clinically mimicking Lemierre’s syndrome. J Med Microbiol 2008, 57:118-120.
  • [28]Burton MJ, Shah P, Swiatlo E: Community-acquired methicillin resistant Staphylococcus aureus as a cause of Fournier’s gangrene. J Med Sci 2008, 335:327-328.
  • [29]Dumitrescu O, Boisset S, Badiou C, Bes M, Benito Y, Reverdy ME, Vandenesch F, Etienne J, Lina G: Effect of antibiotics on Staphylococcus aureus producing Panton-Valentine leukocidin. Antimicrob Agents Chemother 2007, 51:1515-1519.
  • [30]Deleo FR, Otto M, Kreiswirth BN, Chambers HF: Community-associated meticillin-resistant Staphylococcus aureus. Lancet 2010, 375:1557-1568.
  • [31]Deurenberg RH, Stobberingh EE: The evolution of Staphylococcus aureus. Inf Genet Evol 2008, 8:747-763.
  • [32]Holmes NE, Johnson PD, Howden BP: Relationship between Vancomycin-Resistant Staphylococcus aureus, Vancomycin-Intermediate S. aureus, High Vancomycin MIC, and Outcome in Serious S. aureus Infections. J Clin Microbiol 2012, 50:2548-2552.
  • [33]Hiramatsu K, Aritaka N, Hanaki H, Kawasaki S, Hosoda Y, Kobayashi I: Dissemination in Japanese hospitals of strains of S. aureus heterogeneously resistant to vancomycin. Lancet 1997, 350:1670-1673.
  • [34]Denton M, O'Connell B, Bernard P, Jarlier V, Wiliams Z, Santerre Henriksen A: The EPISA Study: antimicrobial susceptibility of Staphylococcus aureus causing primary or secondary skin and soft tissue infections in the community in France, the UK and Ireland. J Antimicrobial Chemother 2008, 61(3):586-588.
  • [35]Elazhari M, Saile R, Dersi N, Timinouni M, Elmalki A, Zriouil SB, Hassar M, Zerouali K: Activité de 16 Antibiotiques vis-à-vis des Staphylococcus aureus communautaires à Casablanca (Maroc) et Prévalence des Souches Résistantes à la Méthicilline. Eur J Sci Res 2009, 30:128-137.
  • [36]Cohen ML: Epidemiology of drug resistance: implications for a post-antimicrobial era. Science 1992, 257:1050-1055.
  • [37]Sina H, Baba-Moussa F, Ahoyo TA, Mousse W, Anagonou S, Gbenou JD, Prévost G, Kotchoni SO, Baba-Moussa L: Antibiotic susceptibility and Toxins production of Staphylococcus aureus isolated from clinical samples from Benin. Afr J Microbiol Res 2011, 5:2797-2808.
  • [38]Randrianirina F, Soares JL, Ratsima E, Carod JF, Combe P, Grosjean P, Richard V, Talarmin A: In vitro activities of 18 antimicrobial agents against Staphylococcus aureus isolates from the Institut Pasteur of Madagascar. Ann Clin Microbiol Antimicrob 2007, 6:5.
  • [39]Kesah C, Ben Redjeb S, Odugbemi TO, Boye CS, Dosso M, Ndinya Achola JO, Koulla-Shiro S, Benbachir M, Rahal K, Borg M: Prevalence of methicillin-resistant Staphylococcus aureus in eight African hospitals and Malta. Clin Microbiol Infect 2003, 9:153-156.
  • [40]Baba-Moussa L, Sanni A, Dagnra AY, Anagonou S, Prince-David M, Edoh V, Befort JJ, Prévost G, Monteil H: Approche épidémiologique de l'antibiorésistance et de la production de leucotoxines par les souches de Staphylococcus aureus isolées en Afrique de l'Ouest. Med Mal Infect 1999, 29(11):689-696.
  • [41]Diekema DJ, Pfaller MA, Schmitz FJ, Smayevsky J, Bell J, Jones RN, Beach M: Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997–1999. Clin Infect Dis 2001, 32(suppl 2):114-132.
  • [42]Belabbès H, Elmdaghri N, Hachimi K, Marih L, Zerouali K, Benbachir M: Résistance de Staphylococcus aureus isolé des infections communautaires et hospitalieres à Casablanca. Communication brève. Med Mal Infect 2001, 31:25-28.
  • [43]Maor Y, Hagin M, Belausov N, Keller N, Ben-David D, Rahav G: Clinical features of heteroresistant vancomycin-intermediate Staphylococcus aureus bacteremia versus those of methicillin-resistant S. aureus bacteremia. J Infect Dis 2009, 199:619-624.
  • [44]Okon KO, Uba A, Oyawoye OM, Yusuf IZ, Adesina OO: Prevalence and Antibiotic susceptibility pattern of Panton-Valentine Leucocidin (PVL) positive Staphylococcus aureus Strains from clinical specimens in Northeastern Nigeria. Sierra Leone J Biomed Res 2012, 4(1):43-52.
  • [45]Aires de Sousa M, Conceicao T, de Lancastre H: Unusually high prevalence of nosocomial Panton-Valentine leukocidin –positive Staphylococcus aureus isolates in Cape Verdes Island. J Clin Microbiol 2006, 44:37-3793.
  • [46]Campbell SJ, Deshmukl HS, Nelson CL, Bae I: Genotypic characterization of Staphylococcus aureus isolates from a multinational trial of topical drugs for skin and skin stricture infections. J Clin Microbiol 2008, 46:678-684.
  • [47]Goering RV, Shawar RM, Scangarella NE, OHara FP, Amrine-Madsen H, West JM, Dalessandro M, Becker JA, Walsh SL, Miller LA, van Horn SF, Thomas ES, Twynholm T: Molecular epidemiology of methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from global clinical trial. J Clin Microbiol 2008, 9:2842-2847.
  • [48]Prévost G, Mourey L, Colin DA, Menestrina G: Staphylococcal pore-forming toxins. Curr Top Microbiol Immunol 2001, 257:53-83.
  • [49]Genestier AL, Michallet MC, Prevost G, Bellot G, Chalabreysse L, Peyrol S, Thivolet F, Etienne J, Lina G, Vallette FM, Vandenesch F, Genestier L: Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. J Clin Invest 2005, 115:3117-3127.
  • [50]Ladhani S: Understanding the mechanism of action of the exfoliative toxins of Staphylococcus aureus. FEMS Immunol Med Microbiol 2003, 39:181-189.
  • [51]Prevost G, Couppie P, Monteil H: Staphylococcal epidermolysins. Curr Opin Infect Dis. 2003, 16:71-76.
  • [52]Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, Liassine N, Bes M, Greenland T, Reverdy ME, Etienne J: Community acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 2003, 9:978-984.
  • [53]Morris CA, Conway HD, Everall PH: Food-poisoning due to staphylococcal enterotoxin E. Lancet 1972, 2:1375-1376.
  • [54]Chen TR, Chiou CS, Tsen HY: Use of Novel PCR Primers Specific to the Genes of Staphylococcal Enterotoxin G, H, I for the Survey of Staphylococcus aureus Strains Isolated From Food-Poisoning Cases and Food Samples in Taiwan. Int J Food Microbiol 2004, 92:189-197.
  • [55]Ikeda T, Tamate N, Yamaguchi K, Makino S: Mass Outbreak of Food Poisoning Disease Caused by Small Amounts of Staphylococcal Enterotoxins A and H. Appl Environ Microbiol 2005, 71:2793-2795.
  • [56]Daum RS, Ito T, Hiramatsu K, Hussain F, Mongkolrattanothai K, Jamklang M, Boyle-Vavra S: A novel methicillin-resistance cassette in community-acquired methicillin-resistant Staphylococcus aureus isolates of diverse genetic backgrounds. J Infect Dis 2002, 186:1344-1347.
  • [57]Naimi TS, LeDell KH, Como-Sabetti K, et al.: Comparison of com-munity- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 2003, 290:2976-2984.
  • [58]Buckingham SC, McDougal LK, Cathey LD, et al.: Emergence of com-munity-associated methicillin-resistant Staphylococcus aureus at a Memphis, Tennessee Children’s Hospital. Pediatr Infect Dis J 2004, 23:619-624.
  • [59]Cosgrove SE, Sakoulas G, Perencevich EN, Schwaber MJ, Karchmer AW, Carmeli Y: Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 2003, 36:53-59.
  • [60]Bergdoll MS, Crass BA, Reiser RF, Robbins RN, Davis JP: A New Staphylococcal Enterotoxin, Enterotoxin F, Associated with Toxic-Shock-Syndrome Staphylococcus aureus Isolates. Lancet 1981, 1:1017-1021.
  • [61]Baldwin LN, Lowe AD: Panton-Valentine Leukocidin associated with community acquired methicillin resistant Staphylococcus aureus: a case report and review of interim guidelines. Anaesthesia 2008, 63:764-766.
  • [62]Chambers HF: Methicillin resistance in staphylococci: molecular and biochemical basis and clinical implications. Clin Microbiol Rev 1997, 10:781-791.
  • [63]Labischinski H: Consequences of the interaction of beta-lactam antibiotics with penicillin binding proteins from sensitive and resistant Staphylococcus aureus strains. Med Microbiol Immunol 1992, 181:241-265.
  • [64]Cheesbrough M: District Laboratory Practice in Tropical Countries: Part 2. Cambridge, UK: Cambridge University Press; 2004:299-329.
  • [65]Société Française de Microbiologie: Recommandations du Comité de l’Antibiogramme de la Société Française de Microbiologie. 2012. http://www.sfm-microbiologie.org/UserFiles/file/CASFM/CASFM_2012.pdf webcite
  • [66]Clinical and Laboratory Standards Institute: Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, Approved standard. 8th edition. Document M7-A8. Clinical and Laboratory Standards Institute Wayne: PA; 2009.
  • [67]Gauduchon V, Werner S, Prévost G, Monteil H, Colin DA: Flow cytometric determination of Panton-Valentine leucocidin S component binding. Infect Immun 2001, 69:2390-2395.
  • [68]Prévost G, Couppie P, Prévost P, Gayet S, Petiau P, Cribier B, Monteil H, Piemont Y: Epidemiological data on Staphylococcus aureus strains producing synergohymenotropic toxins. J Med Microbiol 1995, 42:237-245.
  • [69]Gravet A, Colin DA, Keller D, Girardot R, Monteil H, Prevost G: Characterization of a novel structural member, LukE-LukD, of the bi-component staphylococcal leucotoxins family. FEBS Lett 1998, 436:202-208.
  • [70]Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, Nesme X, Etienne J, Vandenesch F: Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 2002, 70:631-641.
  • [71]Joubert O, Keller D, Pinck A, Monteil H, Prevost G: Sensitive and specific detection of staphylococcal epidermolysins A and B in broth cultures by flow cytometry-assisted multiplex immunoassay. J Clin Microbiol 2005, 43:1076-1080.
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