• 1.

    Kluytmans JA, van Belkum A, Verbrugh HA, 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10: 505520.

    • Search Google Scholar
    • Export Citation
  • 2.

    Alvarez JA, Ramirez AJ, Mojica-Larrea M, Huerta J del R, Guerrero JD, Rolon AL, Medina H, Munoz JM, Mosqueda JL, Macias AE, Sifuentes-Osornio J, 2009. Methicillin-resistant Staphylococcus aureus at a general hospital: epidemiological overview between 2000 and 2007. Rev Invest Clin 61: 98103.

    • Search Google Scholar
    • Export Citation
  • 3.

    Burlage RS, Mahdi N, 2009. A novel molecular pattern for methicillin-resistant Staphylococcus aureus in Milwaukee, WI clinical isolates. Diagn Microbiol Infect Dis 63: 296301.

    • Search Google Scholar
    • Export Citation
  • 4.

    Choi CS, Yin CS, Bakar AA, Sakewi Z, Naing NN, Jamal F, Othman N, 2006. Nasal carriage of Staphylococcus aureus among healthy adults. J Microbiol Immunol Infect 39: 458464.

    • Search Google Scholar
    • Export Citation
  • 5.

    Grundmann HA, Aires-de-Sousa M, Boyce J, Tiemersma E, 2006. Emergence and resurgence of methicillin-resistant Staphylococcus aureus as a public health threat. Lancet 368: 874875.

    • Search Google Scholar
    • Export Citation
  • 6.

    Johnston BL, Bryce E, 2009. Hospital infection control strategies for vancomycin-resistant enterococcus, methicillin-resistant Staphylococcus aureus and Clostridium difficile. CMAJ 180: 627631.

    • Search Google Scholar
    • Export Citation
  • 7.

    Kwon JC, Kim SH, Park SH, Choi SM, Lee DG, Choi JH, Park C, Shin NY, Yoo JH, 2011. Molecular epidemiologic analysis of methicillin-resistant Staphylococcus aureus isolates from bacteremia and nasal colonization at 10 intensive care units: multicenter prospective study in Korea. J Korean Med Sci 26: 604611.

    • Search Google Scholar
    • Export Citation
  • 8.

    Zinn CS, Westh H, Rosdahl VT; the Sarisa Study Group, 2004. An international multicenter study of antimicrobial resistance and typing of hospital Staphylococcus aureus isolates from 21 laboratories in 19 countries or states. Microb Drug Resist 10: 160168.

    • Search Google Scholar
    • Export Citation
  • 9.

    Ben-David DM, Parenteau S, 2008. Methicillin-resistant Staphylococcus aureus transmission: the possible importance of unrecognized health care worker carriage. Am J Infect Control 36: 9397.

    • Search Google Scholar
    • Export Citation
  • 10.

    Davis KA, Stewart JJ, Crouch HK, Florez CE, Hospenthal DR, 2004. Methicillin-resistant Staphylococcus aureus (MRSA) nares colonization at hospital admission and its effect on subsequent MRSA infection. CID 39: 776782.

    • Search Google Scholar
    • Export Citation
  • 11.

    Fishbain JT, Lee JC, Nguyen HD, Mikita JA, Mikita CP, Uyehara CF, Hosphental DR, 2003. Nosocomial transmission of methicillin-resistant Staphylococcus aureus: a blinded study to establish baseline acquisition rates. Infect Control Hosp Epidemiol 24: 415421.

    • Search Google Scholar
    • Export Citation
  • 12.

    Lucet JC, Paoletti X, Demontpion C, Degrave M, Vanjak D, Vincent C, Andremont A, Jarlier V, Mentre F, Nicolas-Chanoine MH, 2009. Carriage of methicillin-resistant Staphylococcus aureus in home care settings: prevalence, duration, and transmission to household members. Arch Intern Med 169: 13721378.

    • Search Google Scholar
    • Export Citation
  • 13.

    Moore C, Dhaliwal J, Tong A, Eden S, Wigston C, Willey B, McGeer A, 2008. Risk factors for methicillin-resistant Staphylococcus aureus (MRSA) acquisition in roommate contacts of patients colonized or infected with MRSA in an acute-care hospital. Infect Control Hosp Epidemiol 29: 600606.

    • Search Google Scholar
    • Export Citation
  • 14.

    Boyce JM, 2007. Environmental contamination makes an important contribution to hospital infection. J Hosp Infect 65: 5054.

  • 15.

    Hardy KJ, Oppenheim BA, Gossain S, Gao F, Hawkey PM, 2006. A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients' acquisition of MRSA. Infect Control Hosp Epidemiol 27: 127132.

    • Search Google Scholar
    • Export Citation
  • 16.

    Sexton T, Clarke P, O'Neill E, Dillane T, Humphreys H, 2006. Environmental reservoirs of methicillin-resistant Staphylococcus aureus in isolation rooms: correlation with patient isolates and implications for hospital hygiene. J Hosp Infect 62: 187194.

    • Search Google Scholar
    • Export Citation
  • 17.

    Shigeharu O, Suenaga S, Sawa A, Kamiya A, 2007. Association between isolation sites of methicillin-resistant Staphylococcus aureus (MRSA) in patients with MRSA-positive body sites and MRSA contamination in their surrounding environmental surfaces. Jpn J Infect Dis 60: 367369.

    • Search Google Scholar
    • Export Citation
  • 18.

    Aizen E, Ljubuncic Z, Ljubuncic P, Aizen I, Potasman I, 2007. Risk factors for methicillin-resistant Staphylococcus aureus colonization in a geriatric rehabilitation hospital. J Gerontol A Biol Sci Med Sci 62: 11521156.

    • Search Google Scholar
    • Export Citation
  • 19.

    Lestari ES, Severin JA, Fillus PMG, Kuntaman K, Duerink DO, Hadi U, Wahjono H, Verbrugh HA, 2008. Antimicrobial resistance among commensal isolates of Escherichia coli and Staphylococcus aureus in the Indonesian population inside and outside hospitals. Eur J Clin Microbiol Infect Dis 27: 4551.

    • Search Google Scholar
    • Export Citation
  • 20.

    Severin JA, Lestari ES, Kuntaman K, Melles DC, Pastink M, Peeters JK, Snijders SV, Hadi U, Duerink DO, van Belkum A, Verbrugh HA, 2008. Unusually high prevalence of Panton-Valentine leukocidin genes among methicillin-sensitive Staphylococcus aureus strains carried in the Indonesian population. J Clin Microbiol 46: 19891995.

    • Search Google Scholar
    • Export Citation
  • 21.

    Lina G, Plemont Y, Godall-Gamot F, Bes M, Peter M-O, Gauduchon V, Vandenesch F, Etienne J, 1999. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. CID 29: 11281132.

    • Search Google Scholar
    • Export Citation
  • 22.

    Melles DC, Gorkink RF, Boelens HA, Snijders SV, Peeters JK, Moorhouse MJ, van der Spek PJ, van Leeuwen WB, Simons G, Verbrugh HA, van Belkum A, 2004. Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus. J Clin Invest 114: 17321740.

    • Search Google Scholar
    • Export Citation
  • 23.

    Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S, 1991. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol 29: 22402244.

    • Search Google Scholar
    • Export Citation
  • 24.

    Milheirico C, Oliveira DC, de Lencastre H, 2007. Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus. Antimicrob Agents Chemother 51: 33743377.

    • Search Google Scholar
    • Export Citation
  • 25.

    Te Witt R, Vaessen N, Melles DC, Lekkerkerk WS, van der Zwaan EA, Zandijk WH, Severin JA, Vos MC, 2013. Good performance of SpectraCellRA system for typing of methicillin-resistant Staphylococcus aureus (MRSA). J Clin Microbiol 51: 14341438.

    • Search Google Scholar
    • Export Citation
  • 26.

    Willemse-Erix DF, Scholtes-Timmerman MJ, Jachtenberg JW, van Leeuwen WB, Horst-Kreft D, Bakker Schut TC, Deurenberg RH, Puppels GJ, van Belkum A, Vos MC, Maquelin K, 2009. Optical fingerprinting in bacterial epidemiology: Raman spectroscopy as a real-time typing method. J Clin Microbiol 47: 652659.

    • Search Google Scholar
    • Export Citation
  • 27.

    Willemse-Erix D, Bakker-Schut T, Slagboom-Bax F, Jachtenberg JW, Toom NL, Papagiannitsis CC, Kuntaman K, Puppels G, van Belkum A, Severin J, Goessens W, Maquelin K, 2012. Rapid typing of extended-spectrum beta-lactamase- and carbapenemase- producing Escherichia coli and Klebsiella pneumoniae isolates by use of spectraCell RA. J Clin Microbiol 50: 13701375.

    • Search Google Scholar
    • Export Citation
  • 28.

    Enright MC, Day NPJ, Davies CE, Peacock SJ, Spratt BG, 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38: 10081015.

    • Search Google Scholar
    • Export Citation
  • 29.

    Lestari ES, Duerink DO, Hadi U, Severin JA, Nagerlkerke NJ, Kuntaman K, Wahjono H, Gardjito W, Soejoenoes A, van den Broek PJ, Keuter M, Gyssens IC, Verbrugh HA, 2010. Determinants of carriage of resistant Staphylococcus aureus among S. aureus carriers in the Indonesian population inside and outside hospitals. Trop Med Int Health 15: 12351243.

    • Search Google Scholar
    • Export Citation
  • 30.

    Cooper BS, Batra R, Wyncoll D, Tosas O, Edgeworth JD, 2012. Quantifying type-specific reproduction numbers for nosocomial pathogens: evidence for heightened transmission of an Asian sequence Type 239 MRSA clone. PLOS Computational Biology 8: 113.

    • Search Google Scholar
    • Export Citation
  • 31.

    Severin JA, Lestari ES, Kuntaman K, Pastink M, Snijders SV, Toom NL, Horst-Kreft D, Hadi U, Duerink DO, Goessens WH, Fluit AC, van Wamel W, van Belkum A, Verbrugh HA, 2010. Nasal carriage of methicillin-resistant and methicillin sensitive strains of Staphylococcus sciuri in the Indonesian population: epidemiology and risk factors. Antimicrob Agents Chemother 54: 54135417.

    • Search Google Scholar
    • Export Citation
  • 32.

    Jariyasethpong T, Tribuddharat C, Dejsirilert S, Kerdsin A, Tishyadhigama P, Rahule S, Sawanpanyalert P, Yosapol P, Aswapokee N, 2010. MRSA carriage in a tertiary governmental hospital in Thailand: emphasis on prevalence and molecular epidemiology. Eur J Clin Microbiol Infect Dis 29: 977985.

    • Search Google Scholar
    • Export Citation
  • 33.

    Mathanraj S, Sujatha S, Sivasangeetha K, Parija SC, 2009. Screening for methicillin-resistant Staphylococcus aureus carriers among patients and health care workers of a tertiary care hospital in south India. Indian J Med Microbiol 27: 6264.

    • Search Google Scholar
    • Export Citation
  • 34.

    Sivaraman K, Venkataraman N, Cole AM, 2009. Staphylococcus aureus nasal carriage and its contributing factors. Future Microbiol 4: 9991008.

  • 35.

    Tacconelli E, De Angelis G, Cataldo MA, Mantengoli E, Spanu T, Pan A, Corti G, Radice A, Stolzuoli L, Antinori S, Paradisi F, Carosi G, Bernabei R, Antonelli M, Fadda G, Rossolini GM, Cauda R, 2009. Antibiotic usage and risk of colonization and infection with antibiotic-resistant bacteria a hospital population-based study. Antimicrob Agents Chemother 53: 42644269.

    • Search Google Scholar
    • Export Citation
  • 36.

    Deurenberg RH, Beisser PS, Visschers MJ, Driessen C, Stobberingh EE, 2010. Molecular typing of methicillin-susceptible Staphylococcus aureus isolates collected in the Yogyakarta area in Indonesia, 2006. Clin Microbiol Infect 16: 9294.

    • Search Google Scholar
    • Export Citation
  • 37.

    Neela VK, Ehsanollah GR, Zamberi S, van Belkum A, Mariana NS, 2009. Prevalence of Panton-Valentine leukocidin genes among carriage and invasive Staphylococcus aureus isolates in Malaysia. Int J Infect Dis 13: e131e132.

    • Search Google Scholar
    • Export Citation
  • 38.

    Boyle-Vavra S, Daum RS, 2007. Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab Invest 87: 39.

    • Search Google Scholar
    • Export Citation
  • 39.

    Gurieva T, Bootsma MC, Bonten MJ, 2013. Cost and effects of different admission screening strategies to control the spread of methicillin-resistant Staphylococcus aureus. PLOS Comput Biol 9: 111.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Epidemiology of Staphylococcus aureus Harboring the mecA or Panton-Valentine Leukocidin Genes in Hospitals in Java and Bali, Indonesia

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  • Department of Microbiology, Faculty of Medicine, Brawijaya University/Dr. Saiful Anwar Hospital, Malang, Indonesia; Department of Microbiology, Faculty of Medicine, Udayana University/Sanglah Hospital, Denpasar, Bali, Indonesia; Department of Microbiology, Faculty of Medicine, Airlangga University/Dr. Soetomo Hospital, Surabaya, Indonesia; Department of Microbiology, Faculty of Medicine, Diponegoro University/Dr. Kariadi Hospital, Semarang, Indonesia; Laboratory of Molecular Genetics, Instituto de Tecnologia Quimica e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal; Center for Optical Diagnostics and Therapy, Department of Dermatology, Erasmus University Medical Center, Rotterdam, The Netherlands; Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center, Rotterdam, The Netherlands

Data of Staphylococcus aureus carriage in Indonesian hospitals are scarce. Therefore, the epidemiology of S. aureus among surgery patients in three academic hospitals in Indonesia was studied. In total, 366 of 1,502 (24.4%) patients carried S. aureus. The methicillin-resistant S. aureus (MRSA) carriage rate was 4.3%, whereas 1.5% of the patients carried Panton-Valentine leukocidin (PVL)-positive methicillin-sensitive S. aureus (MSSA). Semarang and Malang city (odds ratio [OR] 9.4 and OR 9.0), being male (OR 2.4), hospitalization for more than 5 days (OR 11.708), and antibiotic therapy during hospitalization (OR 2.6) were independent determinants for MRSA carriage, whereas prior hospitalization (OR 2.5) was the only one risk factor for PVL-positive MSSA carriage. Typing of MRSA strains by Raman spectroscopy showed three large clusters assigned type 21, 24, and 38, all corresponding to ST239-MRSA-SCCmec type III. In conclusion, MRSA and PVL-positive MSSA are present among patients in surgical wards in Indonesian academic hospitals.

Author Notes

* Address correspondence to Dewi Santosaningsih, Department of Microbiology, Faculty of Medicine, Brawijaya University, Jl. Veteran, Malang, Indonesia 65145. E-mail: dewi_santosa@yahoo.com

Financial support: This study was supported by the Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center, Rotterdam, The Netherlands and by RUTI grant no. RUTI: SK Menristek No. 97/M/Kp/XI/2007, No. 194/M/Kp/X/2008, and No.110/M/Kp/X/2009 from the Ministry of Research and Technology, Republic of Indonesia.

Authors' addresses: Dewi Santosaningsih and Sanarto Santoso, Department of Microbiology, Faculty of Medicine, Brawijaya University/Dr. Saiful Anwar Hospital, Malang, Indonesia, E-mails: dewi_santosa@yahoo.com and sanarto_santoso@binamandiri.com. Nyoman S. Budayanti, Department of Microbiology, Faculty of Medicine, Udayana University/Sanglah Hospital, Denpasar, Bali, Indonesia, E-mail: nyomansribudayanti@gmail.com. Kuntaman Kuntaman, Department of Microbiology, Faculty of Medicine, Airlangga University/Dr. Soetomo Hospital, Surabaya, Indonesia, E-mail: k.kuntaman@yahoo.com. Endang S. Lestari, Helmia Farida, Rebriarina Hapsari, Purnomo Hadi, and Winarto Winarto, Department of Microbiology, Faculty of Medicine, Diponegoro University/Dr. Kariadi Hospital, Semarang, Indonesia, E-mails: endang_sri_lestari@yahoo.com, helmia_farida@yahoo.com, happy_indonesia@yahoo.com, punknomo@yahoo.com, and winartodip@yahoo.com. Catarina Milheiriço, Laboratory of Molecular Genetics, Instituto de Tecnologia Quimica e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal, E-mail: cicm@itqb.unl.pt. Kees Maquelin and Diana Willemse-Erix, Department of Dermatology, Erasmus University Medical Center, Rotterdam, The Netherlands, E-mails: k.maquelin@erasmusmc.nl and DWillemse@riverd.com. Alex van Belkum, Microbiology Unit, bioMérieux, Inc., La Balme, France, E-mail: alex.vanbelkum@biomerieux.com. Juliëtte A. Severin and Henri A. Verbrugh, Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center, Rotterdam, The Netherlands, E-mails: j.severin@erasmusmc.nl and h.a.verbrugh@erasmusmc.nl.

Reprint requests: Dewi Santosaningsih, Department of Microbiology, Faculty of Medicine, Brawijaya University, Jl. Veteran, Malang, Indonesia, E-mails: dewi_santosa@yahoo.com or dewisantosaningsih@gmail.com.

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