Methicillin-Resistant Staphylococcus aureus Ocular Infection in Taiwan: Potential Role of Panton–Valentine Leukocidin Gene

Purpose The relationship between Panton–Valentine leucocidin (PVL), a major virulence factor of Staphylococcus aureus, and disease severity and clinical outcomes remains unclear. We investigated the molecular characteristics and role of the PVL gene in methicillin-resistant S. aureus (MRSA) ocular infection in Taiwan. Methods Patients with culture-proven S. aureus ocular infection in Chang Gung Memorial Hospital from 2010 to 2017 were included. The presence of the PVL gene was detected for all S. aureus isolates. MRSA isolates were characterized through pulsed-field gel electrophoresis (PFGE), staphylococcal multilocus sequence type, and staphylococcal cassette chromosome mec (SCCmec) typing. Drug susceptibility was examined using disk diffusion method and E-test. Patients’ demographics, diagnoses, and outcomes were collected. Results There were 112 methicillin-sensitive S. aureus and 103 MRSA isolates. Among 50 PVL(+) S. aureus isolates, 43 were MRSA. CC59/PFGE type D/SCCmec IV, VT (38 of 43 isolates, 88%), and CC59/PFGE type C/SCCmec IV (27 of 60 isolates, 45%) were the predominant clones in the PVL(+) and PVL(−) MRSA isolates, respectively. When we compared the two CC59 strains, the patients with PVL(+)/CC59 MSRA infection were significantly younger than those with PVL(−)/CC59 MSRA (39.3 vs. 61.7 years; P = 0.001). PVL(+)/CC59 MSRA caused significantly more eyelid disorders (36.8% vs. 3.7%; P = 0.002) but less keratitis (23.7% vs. 51.9%; P = 0.034). The antibiograms of the two strains were similar. Conclusions PVL(+) MRSA is significantly associated with eyelid infection, especially in young patients. Translational Relevance PVL gene plays a role in clinical features of MRSA ocular infections.

[1]  M. Gilmore,et al.  Hospital-Associated Multidrug-Resistant MRSA Lineages Are Trophic to the Ocular Surface and Cause Severe Microbial Keratitis , 2020, Frontiers in Public Health.

[2]  P. Asbell,et al.  Antibiotic resistance among ocular pathogens: current trends from the ARMOR surveillance study (2009–2016) , 2019, Clinical optometry.

[3]  S. Kaplan,et al.  Molecular Characterization of Staphylococcus aureus Isolates From Children With Periorbital or Orbital Cellulitis , 2018, Journal of the Pediatric Infectious Diseases Society.

[4]  S. Cosgrove,et al.  Trends in Methicillin-Resistant Staphylococcus aureus Hospitalizations in the United States, 2010-2014 , 2017, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[5]  Yhu-Chering Huang,et al.  Methicillin-Resistant Staphylococcus aureus Ocular Infection in Taiwan , 2015, Medicine.

[6]  C. Unger,et al.  Characterization and Comparison of 2 Distinct Epidemic Community-Associated Methicillin-Resistant Staphylococcus aureus Clones of ST59 Lineage , 2013, PloS one.

[7]  Yhu-Chering Huang,et al.  Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Asia. , 2013, The Lancet. Infectious diseases.

[8]  S. Tuft,et al.  lukSF-PV in Staphylococcus aureus keratitis isolates and association with clinical outcome. , 2013, Investigative ophthalmology & visual science.

[9]  Anne M Johnson,et al.  The role of the Panton-Valentine leucocidin toxin in staphylococcal disease: a systematic review and meta-analysis , 2013, The Lancet. Infectious diseases.

[10]  Yhu-Chering Huang,et al.  Methicillin-resistant Staphylococcus aureus ocular infection: a 10-year hospital-based study. , 2012, Ophthalmology.

[11]  T. Morris,et al.  Monitoring antibiotic resistance in ocular microorganisms: results from the Antibiotic Resistance Monitoring in Ocular micRorganisms (ARMOR) 2009 surveillance study. , 2011, American journal of ophthalmology.

[12]  Yhu-Chering Huang,et al.  Community-associated meticillin-resistant Staphylococcus aureus in children in Taiwan, 2000s. , 2011, International journal of antimicrobial agents.

[13]  S. Hopkins,et al.  Panton-Valentine leukocidin associated staphylococcal disease: a cross-sectional study at a London hospital, England. , 2010, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[14]  Chih-Chien Wang,et al.  Panton-Valentine leukocidin is associated with exacerbated skin manifestations and inflammatory response in children with community-associated staphylococcal scarlet fever. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[15]  L. Su,et al.  Comparative molecular analysis of community-associated and healthcare-associated methicillin-resistant Staphylococcus aureus isolates from children in northern Taiwan. , 2008, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[16]  B. Diep,et al.  The role of virulence determinants in community-associated MRSA pathogenesis. , 2008, Trends in microbiology.

[17]  Wei-Jen Lin,et al.  Risk Factors and Molecular Analysis of Panton-Valentine Leukocidin-Positive Methicillin-Resistant Staphylococcus aureus Colonization in Healthy Children , 2008, The Pediatric infectious disease journal.

[18]  M. Raizman,et al.  Ocular TRUST: nationwide antimicrobial susceptibility patterns in ocular isolates. , 2008, American journal of ophthalmology.

[19]  E. Delong,et al.  Staphylococcus aureus Panton-Valentine Leukocidin Causes Necrotizing Pneumonia , 2007, Science.

[20]  Loren G. Miller,et al.  Community-associated Methicillin-resistant Staphylococcus aureus Isolates and Healthcare-Associated Infections , 2007, Emerging infectious diseases.

[21]  Xiao Xue Ma,et al.  Combination of Multiplex PCRs for Staphylococcal Cassette Chromosome mec Type Assignment: Rapid Identification System for mec, ccr, and Major Differences in Junkyard Regions , 2006, Antimicrobial Agents and Chemotherapy.

[22]  R. Weinstein,et al.  Community-associated Methicillin-resistant Staphylococcus aureus , 2006, Emerging infectious diseases.

[23]  Tina Rutar,et al.  Ophthalmic manifestations of infections caused by the USA300 clone of community-associated methicillin-resistant Staphylococcus aureus. , 2006, Ophthalmology.

[24]  R. Willems,et al.  Emergence of Virulent Methicillin-Resistant Staphylococcus aureus Strains Carrying Panton-Valentine Leucocidin Genes in The Netherlands , 2005, Journal of Clinical Microbiology.

[25]  G. Horsman,et al.  Community-associated Methicillin-resistant Staphylococcus aureus, Canada , 2005, Emerging infectious diseases.

[26]  S. Deresinski Methicillin-resistant Staphylococcus aureus: an evolutionary, epidemiologic, and therapeutic odyssey. , 2005, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[27]  F. Vandenesch,et al.  Community-Acquired Methicillin-Resistant Staphylococcus aureus Carrying Panton-Valentine Leukocidin Genes: Worldwide Emergence , 2003, Emerging infectious diseases.

[28]  P. Vanhems,et al.  Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients , 2002, The Lancet.

[29]  M. Ferraro Performance standards for antimicrobial susceptibility testing , 2001 .

[30]  Nicholas P. J. Day,et al.  Multilocus Sequence Typing for Characterization of Methicillin-Resistant and Methicillin-Susceptible Clones ofStaphylococcus aureus , 2000, Journal of Clinical Microbiology.

[31]  B. Spratt,et al.  Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. , 2000, Journal of clinical microbiology.

[32]  F. Vandenesch,et al.  Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. , 1999, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.