Methicillin-resistant Staphylococcus aureus: a consensus review of the microbiology, pathogenesis, and epidemiology with implications for prevention and management.

Methicillin-resistant Staphylococcus aureus (MRSA) has become a major nosocomial pathogen in community hospitals, long-term-care facilities, and tertiary care hospitals. The basic mechanism of resistance is alteration in penicillin-binding proteins of the organism. Methods for isolation by culture and typing of the organism are reviewed. MRSA colonization precedes infection. A major reservoir is the anterior nares. MRSA is usually introduced into an institution by a colonized or infected patient or health care worker. The principal mode of transmission is via the transiently colonized hands of hospital personnel. Indications for antibiotic therapy for eradication of colonization and treatment of infection are reviewed. Infection control guidelines and discharge policy are presented in detail for acute-care hospitals, intensive care and burn units, outpatient settings, and long-term-care facilities. Recommendations for handling an outbreak, surveillance, and culturing of patients are presented based on the known epidemiology.

[1]  D. Vlahov,et al.  Prospective Microbiologic Surveillance in Control of Nosocomial Methicillin-Resistant Staphylococcus aureus , 1987, Infection Control.

[2]  P. M. Terry,et al.  Use of plasmid analysis and determination of aminoglycoside-modifying enzymes to characterize isolates from an outbreak of methicillin-resistant Staphylococcus aureus , 1989, Journal of clinical microbiology.

[3]  A. Reboli,et al.  Methicillin-resistant Staphylococcus aureus outbreak at a Veterans' Affairs Medical Center: importance of carriage of the organism by hospital personnel. , 1990 .

[4]  P. Noone,et al.  AMIKACIN RESISTANCE DEVELOPING IN PATIENT WITH PSEUDOMONAS ÆRUGINOSA BRONCHOPNEUMONIA , 1976, The Lancet.

[5]  M. Bittner,et al.  Attemps to eradicate methicillin-resistant Staphylococcus aureus colonization with the use of trimethoprim-sulfamethoxazole, rafampin, and bacitracin , 1988 .

[6]  J. Boyce,et al.  Increasing Occurrence of Methicillin-Resistant Staphylococcus aureus in the United States , 1982, Infection Control.

[7]  B. Hamory,et al.  Control of Epidemic Methicillin-Resistant Staphylococcus aureus , 1990, Infection Control & Hospital Epidemiology.

[8]  R. Lacey Multi-resistant Staphylococcus aureus--a suitable case for inactivity? , 1987, The Journal of hospital infection.

[9]  D. Coleman,et al.  A new methicillin- and gentamicin-resistant Staphylococcus aureus in Dublin: molecular genetic analysis. , 1989, Journal of medical microbiology.

[10]  Fekety Fr THE EPIDEMIOLOGY AND PREVENTION OF STAPHYLOCOCCAL INFECTION. , 1964 .

[11]  R. Hill,et al.  Elimination of nasal carriage of methicillin-resistant Staphylococcus aureus with mupirocin during a hospital outbreak. , 1988, The Journal of antimicrobial chemotherapy.

[12]  ScienceDirect The Antimicrobic newsletter , 1993 .

[13]  M. Terpenning,et al.  Methicillin-Resistant Staphylococcus aureus in Lona-Term Care Facilities , 1990 .

[14]  J. May,et al.  Molecular epidemiology of multiresistant Staphylococcus aureus in Australian hospitals. , 1984, Journal of medical microbiology.

[15]  A. Tomasz,et al.  Expression of methicillin resistance in heterogeneous strains of Staphylococcus aureus , 1986, Antimicrobial Agents and Chemotherapy.

[16]  C. C. Hsu,et al.  Serial Survey of Methicillin-Resistant Staphylococcus aureus Nasal Carriage Among Residents in a Nursing Home , 1991, Infection Control & Hospital Epidemiology.

[17]  W. R. Mccabe,et al.  A large outbreak of infections caused by a strain of Staphylococcus aureus resistant of oxacillin and aminoglycosides. , 1981, The American journal of medicine.

[18]  J. Boyce,et al.  Spurious oxacillin resistance in Staphylococcus aureus because of defective oxacillin disks , 1988, Journal of clinical microbiology.

[19]  M. McNeil,et al.  The epidemiology of methicillin-resistant Staphylococcus aureus , 1985 .

[20]  L. Mcdougal,et al.  Successful use of broth microdilution in susceptibility tests for methicillin-resistant (heteroresistant) staphylococci , 1983, Journal of clinical microbiology.

[21]  M. Goldberg,et al.  Methicillin resistance in staphylococci: an evaluation of conditions for detection. , 1989, Medical laboratory sciences.

[22]  D. Rimland,et al.  Methicillin-resistant Staphylococcus aureus in Veterans Administration Medical Centers , 1987, Infection Control.

[23]  S. Waterman,et al.  Transmission and Control of Methicillin-Resistant Staphylococcus aureus in a Skilled Nursing Facility , 1989, Infection Control & Hospital Epidemiology.

[24]  J. Hamilton-miller,et al.  Methicillin-resistant Staphylococcus aureus. , 1989, The New England journal of medicine.

[25]  D. Musher,et al.  Activity of Tetracycline, Doxycycline, and Minocycline Against Methicillin-Susceptible and -Resistant Staphylococci , 1974, Antimicrobial Agents and Chemotherapy.

[26]  B. Ribner,et al.  Outbreak of multiply resistant Staphylococcus aureus in a pediatric intensive care unit after consolidation with a surgical intensive care unit. , 1989, American journal of infection control.

[27]  M. Sande,et al.  Effect of Rifampin on Nasal Carriage of Staphylococcus aureus , 1975, Antimicrobial Agents and Chemotherapy.

[28]  M. Barber Methicillin-resistant staphylococci , 1961, Journal of clinical pathology.

[29]  K. Lo The susceptibility of staphylococcal hospital strains to methyl-phenyl-isoxazolyl penicillin. , 1962 .

[30]  V. Yu,et al.  Staphylococcus aureus nasal carriage and infection in patients on hemodialysis. Efficacy of antibiotic prophylaxis. , 1986, The New England journal of medicine.

[31]  J. Thys,et al.  Clinical evaluation of teicoplanin for therapy of severe infections caused by gram-positive bacteria , 1986, Antimicrobial Agents and Chemotherapy.

[32]  R. Lacey,et al.  Properties of methicillin‐resistant staphylococci now endemic in Australia , 1982, The Medical journal of Australia.

[33]  P. M. Terry,et al.  Rapid development of ciprofloxacin resistance in methicillin-susceptible and -resistant Staphylococcus aureus. , 1991, The Journal of infectious diseases.

[34]  M. Goetz,et al.  Management and epidemiologic analyses of an outbreak due to methicillin-resistant Staphylococcus aureus. , 1992, The American journal of medicine.

[35]  J. Miller,et al.  Methicillin-resistant staphylococcal colonization and infection in a long-term care facility. , 1991, Annals of internal medicine.

[36]  J. Boyce,et al.  Impact of methicillin-resistant Staphylococcus aureus on the incidence of nosocomial staphylococcal infections. , 1983, The Journal of infectious diseases.

[37]  J. Sheagren,et al.  Staphylococcus aureus carriage rate of patients receiving long-term hemodialysis. , 1978, Archives of internal medicine.

[38]  J. Jorgensen Mechanisms of methicillin resistance in Staphylococcus aureus and methods for laboratory detection. , 1991, Infection control and hospital epidemiology.

[39]  B. Cookson Mupirocin resistance in staphylococci. , 1990, The Journal of antimicrobial chemotherapy.

[40]  J. Hamilton-miller,et al.  Differing activities of quinolones against ciprofloxacin-susceptible and ciprofloxacin-resistant, methicillin-resistant Staphylococcus aureus , 1991, Antimicrobial Agents and Chemotherapy.

[41]  L. Peterson,et al.  Emergence of ciprofloxacin resistance in nosocomial methicillin-resistant Staphylococcus aureus isolates. Resistance during ciprofloxacin plus rifampin therapy for methicillin-resistant S aureus colonization. , 1990, Archives of internal medicine.

[42]  D. Cohn,et al.  Oral rifampin and trimethoprim/sulfamethoxazole therapy in asymptomatic carriers of methicillin-resistant Staphylococcus aureus infections. , 1984, The Western journal of medicine.

[43]  M. Guiguet,et al.  Effectiveness of simple measures to control an outbreak of nosocomial methicillin-resistant Staphylococcus aureus infections in an intensive care unit. , 1990, Infection control and hospital epidemiology.

[44]  D. Rimland,et al.  Gastrointestinal carriage of methicillin-resistant Staphylococcus aureus , 1986, Journal of clinical microbiology.

[45]  J. Hindler,et al.  Impact of prolonged incubation on disk diffusion susceptibility test results for Staphylococcus aureus , 1987, Journal of clinical microbiology.

[46]  G. Stewart Changes in Sensitivity of Staphylococci to Methicillin , 1961, British medical journal.

[47]  M. Matsuhashi,et al.  Expression and inducibility in Staphylococcus aureus of the mecA gene, which encodes a methicillin-resistant S. aureus-specific penicillin-binding protein , 1989, Journal of Bacteriology.

[48]  L. Saravolatz,et al.  Community-acquired methicillin-resistant Staphylococcus aureus infections: a new source for nosocomial outbreaks. , 1982, Annals of internal medicine.

[49]  R. Wenzel,et al.  Methicillin-resistant Staphylococcus aureus--United States. , 1981, MMWR. Morbidity and mortality weekly report.

[50]  Stuart H. Cohen,et al.  A seven-year experience with methicillin-resistant Staphylococcus aureus. , 1991, The American journal of medicine.

[51]  R. Wenzel,et al.  Epidemiology of nosocomial infections caused by methicillin-resistant Staphylococcus aureus. , 1982, Annals of internal medicine.

[52]  Chabbert Ya,et al.  [Staphylococcus strains naturally resistant to methicillin and 5-methyl-3-phenyl-4-iso-oxazolyl-penicillin]. , 1962 .

[53]  M. Terpenning,et al.  Increasing resistance of Staphylococcus aureus to ciprofloxacin , 1990, Antimicrobial Agents and Chemotherapy.

[54]  Diana Brahams,et al.  Confidentiality and under-age girls who seek contraceptive advice. , 1983, Lancet.

[55]  J. Mcgowan Gram-positive bacteria: spread and antimicrobial resistance in university and community hospitals in the USA. , 1988, The Journal of antimicrobial chemotherapy.

[56]  T. Yokota,et al.  Role of an altered penicillin-binding protein in methicillin- and cephem-resistant Staphylococcus aureus , 1985, Antimicrobial Agents and Chemotherapy.

[57]  R. Hill,et al.  In-vitro activity of mupirocin ('pseudomonic acid') against clinical isolates of Staphylococcus aureus. , 1985, The Journal of antimicrobial chemotherapy.

[58]  J. Rahal,et al.  Tourniquets and nosocomial methicillin-resistant Staphylococcus aureus infections. , 1986, The New England journal of medicine.

[59]  G. Trenholme,et al.  In vitro activity of minocycline and rifampin against staphylococci. , 1989, Diagnostic microbiology and infectious disease.

[60]  S L Hansen,et al.  Detection of intrinsically resistant (heteroresistant) Staphylococcus aureus with the Sceptor and AutoMicrobic systems , 1987, Journal of clinical microbiology.

[61]  B. Berger-Bächi,et al.  Autolysis of methicillin-resistant and -susceptible Staphylococcus aureus , 1992, Antimicrobial Agents and Chemotherapy.

[62]  L. Sabath Mechanisms of resistance to beta-lactam antibiotics in strains of Staphylococcus aureus. , 1982, Annals of internal medicine.

[63]  J. Sheagren,et al.  Staphylococcus aureus among insulin-injecting diabetic patients. An increased carrier rate. , 1975, JAMA.

[64]  Bell Sm Recommendations for control of the spread of methicillin-resistant Staphylococcus aureus infection based on 18 years' experience in a group of teaching hospitals. , 1982 .

[65]  L. Mcdougal,et al.  The role of beta-lactamase in staphylococcal resistance to penicillinase-resistant penicillins and cephalosporins , 1986, Journal of clinical microbiology.

[66]  B. Ribner,et al.  Strict Versus Modified Isolation for Prevention of Nosocomial Transmission of Methicillin-Resistant Staphylococcus aureus , 1986, Infection Control.

[67]  A. Reboli,et al.  Epidemic methicillin-gentamicin-resistant Staphylococcus aureus in a neonatal intensive care unit. , 1989, American journal of diseases of children.

[68]  M. Terpenning,et al.  Methicillin-resistant Staphylococcus aureus: colonization and infection in a long-term care facility. , 1991, Annals of internal medicine.

[69]  C. Thornsberry,et al.  The development of antimicrobial resistance in staphylococci. , 1988, The Journal of antimicrobial chemotherapy.

[70]  C. Mullany,et al.  Comparison of the clinical significance of methicillin‐resistant and methicillin‐sensitive Staphylococcus aureus isolations , 1984, The Medical journal of Australia.

[71]  J. Jui,et al.  Community-acquired methicillin-resistant Staphylococcus aureus endocarditis in the Detroit Medical Center. , 1982, Annals of internal medicine.

[72]  B. Cookson,et al.  Mupirocin-resistant Staphylococcus aureus , 1987, The Lancet.

[73]  J. Boyce,et al.  Burn units as a source of methicillin-resistant Staphylococcus aureus infections. , 1983, JAMA.

[74]  S. Smith In vitro comparison of A-56619, A-56620, amifloxacin, ciprofloxacin, enoxacin, norfloxacin, and ofloxacin against methicillin-resistant Staphylococcus aureus , 1986, Antimicrobial Agents and Chemotherapy.

[75]  M. A. Gaston,et al.  Evaluation of electrophoretic methods for typing methicillin-resistant Staphylococcus aureus. , 1988, Journal of medical microbiology.

[76]  R. Arbeit,et al.  Evidence for a clonal origin of methicillin resistance in Staphylococcus aureus. , 1993, Science.

[77]  C. J. Berg,et al.  CHOLINE PRECURSORS AND ALZHEIMER'S DISEASE , 1982, The Lancet.

[78]  C. Watanakunakorn,et al.  Interaction Between Vancomycin and Rifampin Against Staphylococcus aureus , 1981, Antimicrobial Agents and Chemotherapy.

[79]  R. Eng,et al.  Epidemiology of ciprofloxacin resistance among patients with methicillin-resistant Staphylococcus aureus. , 1990, The Journal of antimicrobial chemotherapy.

[80]  M. Mcnicol,et al.  METHICILLIN-RESISTANT STAPHYLOCOCCI IN A GENERAL HOSPITAL. , 1965, The Lancet.

[81]  F. Waldvogel,et al.  Methicillin-resistant strains of Staphylococcus aureus: relation between expression of resistance and phagocytosis by polymorphonuclear leukocytes. , 1979, The Journal of infectious diseases.

[82]  C. Bryan,et al.  Topical Antibiotic Ointments for Staphylococcal Nasal Carriers: Survey of Current Practices and Comparison of Bacitracin and Vancomycin Ointments , 1980, Infection Control.

[83]  M. Jevons,et al.  Cellbenin-resistant staphylococci. , 1961 .

[84]  R. Locksley,et al.  Multiply antibiotic-resistant Staphylococcus aureus: introduction, transmission, and evolution of nosocomial infection. , 1982, Annals of internal medicine.

[85]  G. Duckworth Revised guidelines for the control of epidemic methicillin-resistant Staphylococcus aureus. Report of a combined working party of the Hospital Infection Society and British Society for Antimicrobial Chemotherapy. , 1990, The Journal of hospital infection.

[86]  H. Portier A multicentre, open, clinical trial of a new intravenous formulation of fusidic acid in severe staphylococcal infections. , 1990, The Journal of antimicrobial chemotherapy.

[87]  J. Hughes,et al.  The emergence of methicillin-resistant Staphylococcus aureus infections in United States hospitals. Possible role of the house staff-patient transfer circuit. , 1982, Annals of internal medicine.

[88]  C. O. Solberg A study of carriers of Staphylococcus aureus with special regard to quantitative bacterial estimations. , 1965, Acta medica Scandinavica. Supplementum.

[89]  G. Archer,et al.  Detection of methicillin resistance in staphylococci by using a DNA probe , 1990, Antimicrobial Agents and Chemotherapy.

[90]  J. Forfar,et al.  Effect of hexachlorophane on incidence of staphylococcal and gram-negative infection in the newborn. , 1968, Lancet.

[91]  R. R. Cutler Relationship between antibiotic resistance, the production of "virulence factors", and virulence for experimental animals in Staphylococcus aureus. , 1979, Journal of medical microbiology.

[92]  J. Musser,et al.  Frequent acquisition of multiple strains of methicillin-resistant Staphylococcus aureus by healthcare workers in an endemic hospital environment. , 1990 .

[93]  P. Ruane,et al.  Ciprofloxacin for eradication of methicillin-resistant Staphylococcus aureus colonization. , 1987, The American journal of medicine.

[94]  H. Nieweg,et al.  SPLEEN IN HODGKINS-DISEASE , 1974 .

[95]  R. Auckenthaler,et al.  Early termination of a prospective, randomized trial comparing teicoplanin and flucloxacillin for treating severe staphylococcal infections. , 1987, The Journal of infectious diseases.

[96]  R. Quintiliani,et al.  Treatment of prosthetic valve endocarditis due to methicillin-resistant Staphylococcus aureus with minocycline. , 1990, The Journal of infectious diseases.

[97]  C. Hackbarth,et al.  Methicillin-resistant staphylococci: detection methods and treatment of infections , 1989, Antimicrobial Agents and Chemotherapy.

[98]  M. Jackson,et al.  Rethinking the role of isolation practices in the prevention of nosocomial infections. , 1987, Annals of internal medicine.

[99]  R. Quintiliani,et al.  Clinical, epidemiologic and bacteriologic observations of an outbreak of methicillin-resistant Staphylococcus aureus at a large community hospital. , 1976, The American journal of medicine.

[100]  D. Shanson Clinical relevance of resistance to fusidic acid in Staphylococcus aureus. , 1990, The Journal of antimicrobial chemotherapy.

[101]  Karen A. Jorgensen,et al.  Emergence of Nosocomial Methicillin-Resistant Staphylococcus aureus and Therapy of Colonized Personnel during a Hospital-Wide Outbreak , 1987, Infection Control.

[102]  C. Hackbarth,et al.  Methicillin-resistant staphylococci: genetics and mechanisms of resistance , 1989, Antimicrobial Agents and Chemotherapy.

[103]  L. Verbist,et al.  The antimicrobial activity of fusidic acid. , 1990, The Journal of antimicrobial chemotherapy.

[104]  B. Houwen,et al.  A-DETERMINANT, Y-DETERMINANT AND D-DETERMINANT IN LIVER-CELLS OF HBSAG CARRIERS , 1976 .

[105]  R. Jones,et al.  Detection of staphylococcal resistance to penicillinase-resistant penicillins. A comparison of two widely used disk diffusion methods. , 1989, Diagnostic microbiology and infectious disease.

[106]  J. Hamilton-miller,et al.  WORLD-WIDE ANTIBIOTIC RESISTANCE IN METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS , 1989, The Lancet.

[107]  A. Bisno,et al.  Methicillin-Resistant Staphylococcus Aureus: Interstate Spread of Nosocomial Infections with Emergence of Gentamicin-Methicillin Resistant Strains , 1980, Infection Control.

[108]  J. Burnie,et al.  A comparison of immunoblot and DNA restriction patterns in characterising methicillin-resistant isolates of Staphylococcus aureus. , 1989, Journal of medical microbiology.

[109]  I. Phillips,et al.  Epidemic methicillin-resistant Staphylococcus aureus. , 1988, The Journal of antimicrobial chemotherapy.

[110]  V. Yu,et al.  Staphylococcal infections in the hemodialysis unit: prevention using infection control principles. , 1988, Infection control and hospital epidemiology.

[111]  R. Darouiche,et al.  Eradication of colonization by methicillin-resistant Staphylococcus aureus by using oral minocycline-rifampin and topical mupirocin , 1991, Antimicrobial Agents and Chemotherapy.

[112]  B. Régnier,et al.  [Staphylococcus aureus endocarditis]. , 1987, Archives des maladies du coeur et des vaisseaux.

[113]  J. Roccaforte,et al.  Infection Control for Home Health , 1990, Infection Control & Hospital Epidemiology.

[114]  K. Jensen Methicillin-resistant staphylococci. , 1968, Lancet.

[115]  J. Jorgensen,et al.  Salt-supplemented medium for testing methicillin-resistant staphylococci with newer beta-lactams , 1988, Journal of clinical microbiology.

[116]  Tamer Ma,et al.  Trimethoprim-Sulfamethoxazole Treatment of Multiantibiotic-Resistant Staphylococcal Endocarditis and Meningitis , 1982 .

[117]  H. Dalton,et al.  Outbreak Due to Methicillin- and Rifampin- Resistant Staphylococcus aureus: Epidemiology and Eradication of the Resistant Strain from the Hospital , 1987, Infection Control.

[118]  H. Standiford Methicillin-resistant Staphylococcus aureus Infections: It's Time to Get Tough , 1987, Infection Control.

[119]  M. Law,et al.  Hospital-acquired infection with methicillin-resistant and methicillin-sensitive staphylococci , 1988, Epidemiology and Infection.

[120]  G. E. Smith,et al.  Staphylococcus aureus resistant to mupirocin. , 1988, The Journal of antimicrobial chemotherapy.

[121]  J. Mylotte,et al.  Prospective study of 114 consecutive episodes of Staphylococcus aureus bacteremia. , 1987, Reviews of infectious diseases.

[122]  H. Standiford,et al.  Novobiocin and rifampicin in combination against methicillin-resistant Staphylococcus aureus: an in-vitro comparison with vancomycin plus rifampicin. , 1986, The Journal of antimicrobial chemotherapy.

[123]  D. Cruess,et al.  Methicillin-Resistant Staphylococcus aureus (MRSA): Risk and Outcome of Colonized vs. Infected Patients , 1985, Infection Control.

[124]  J. Gerberding,et al.  Comparison of conventional susceptibility tests with direct detection of penicillin-binding protein 2a in borderline oxacillin-resistant strains of Staphylococcus aureus , 1991, Antimicrobial Agents and Chemotherapy.

[125]  S. Donta,et al.  The efficacy of rifampin as adjunctive therapy in selected cases of staphylococcal endocarditis. , 1978, Chest.

[126]  W. Lane METHICILLIN RESISTANCE IN STAPHYLOCOCCI , 1962, The Medical journal of Australia.

[127]  D. Kernodle,et al.  Borderline susceptibility to antistaphylococcal penicillins is not conferred exclusively by the hyperproduction of beta-lactamase , 1991, Antimicrobial Agents and Chemotherapy.

[128]  T. Korfhagen,et al.  Methicillin-resistant Staphylococcus aureus: experience in a general hospital over four years. , 1982, American journal of epidemiology.

[129]  C. Goodwin,et al.  Control of methicillin-resistant Staphylococcus aureus (MRSA) in an Australian metropolitan teaching hospital complex. , 1985, The Medical journal of Australia.

[130]  J. Hewitt,et al.  The effect of methicillin on skin lesions in guinea-pigs caused by "methicillin-sensitive" and "methicillin-resistant" Staphylococcus aureus. , 1974, Journal of medical microbiology.

[131]  R. Winn,et al.  Observations Relating to an Inter-Hospital Outbreak of Methicillin-Resistant Staphylococcus aureus: Role of Antimicrobial Therapy in Infection Control , 1981, Infection Control.

[132]  L. Joyce,et al.  Cost-Effective Eradication of an Outbreak of Methicillin-Resistant Staphylococcus aureus in a Community Teaching Hospital , 1988, Infection Control & Hospital Epidemiology.

[133]  J. Sheagren,et al.  Increased rate of carriage of Staphylococcus aureus among narcotic addicts. , 1974, The Journal of infectious diseases.

[134]  A. Tomasz,et al.  Stable classes of phenotypic expression in methicillin-resistant clinical isolates of staphylococci , 1991, Antimicrobial Agents and Chemotherapy.

[135]  C. C. Hsu,et al.  High rate of methicillin resistance of Staphylococcus aureus isolated from hospitalized nursing home patients. , 1988, Archives of internal medicine.

[136]  H. Standiford,et al.  Activity of novobiocin against methicillin-resistant Staphylococcus aureus. , 1985, The Journal of antimicrobial chemotherapy.

[137]  G. Mandell,et al.  Characteristics of rifampin-resistant variants obtained from clinical isolates of Staphylococcus aureus , 1981, Antimicrobial Agents and Chemotherapy.

[138]  R. Eng,et al.  Ciprofloxacin therapy for methicillin-resistant Staphylococcus aureus infections or colonizations , 1989, Antimicrobial Agents and Chemotherapy.

[139]  B. Simmons,et al.  Guideline for isolation precautions in hospitals , 1984, American Journal of Infection Control.

[140]  R. Wenzel,et al.  Methicillin-resistant Staphylococcus aureus: introduction and spread within a hospital. , 1980, Annals of internal medicine.

[141]  J. Boyce,et al.  Induction of β-lactamase and methicillin resistance in unusual strains of methicillin-resistant Staphylococcus aureus , 1990 .

[142]  C. Bartzokas,et al.  Control and eradication of methicillin-resistant Staphylococcus aureus on a surgical unit. , 1984, The New England journal of medicine.

[143]  P. Mackowiak,et al.  Ciprofloxacin for methicillin-resistant Staphylococcus aureus infections , 1989, Antimicrobial Agents and Chemotherapy.

[144]  B. Doebbeling,et al.  Elimination of coincident Staphylococcus aureus nasal and hand carriage with intranasal application of mupirocin calcium ointment. , 1991, Annals of internal medicine.

[145]  W. Noble,et al.  Some effects of plasmids coding for antibiotic resistance on the virulence of Staphylococcus aureus. , 1985, British journal of experimental pathology.

[146]  W. Rutala,et al.  Environmental study of a methicillin-resistant Staphylococcus aureus epidemic in a burn unit , 1983, Journal of clinical microbiology.

[147]  P. Courvalin,et al.  Methicillin-resistant staphylococcemia: bacteriological failure of treatment with cephalosporins. , 1970, Antimicrobial agents and chemotherapy.

[148]  M. Terpenning,et al.  Staphylococcus aureus Nasal Colonization in a Nursing Home: Eradication With Mupirocin , 1990, Infection Control & Hospital Epidemiology.

[149]  E. Kaplan,et al.  Staphylococcus aureus endocarditis. Combined therapy with vancomycin and rifampin. , 1978 .

[150]  C. McLaughlin,et al.  Rapid detection (4 h) of methicillin-resistant Staphylococcus aureus by a bioluminescence method , 1988, Journal of clinical microbiology.

[151]  J. Boyce,et al.  Epidemiologie Studies of an Outbreak of Nosocomial Methicillin-Resistant Staphylococcus aureus Infections , 1981, Infection Control.

[152]  K. Crossley,et al.  An outbreak of infections caused by strains of Staphylococcus aureus resistant to methicillin and aminoglycosides. II. Epidemiologic studies. , 1979, The Journal of infectious diseases.

[153]  R. Croton,et al.  Methicillin resistant Staphylococcus aureus; the role of antisepsis in the control of an outbreak. , 1987, The Journal of hospital infection.

[154]  A. Tomasz,et al.  Involvement of multiple genetic determinants in high-level methicillin resistance in Staphylococcus aureus , 1989, Journal of bacteriology.

[155]  R. Wenzel,et al.  Methicillin-resistant Staphylococcus aureus: microbiologic characteristics, antimicrobial susceptibilities, and assessment of virulence of an epidemic strain. , 1981, The Journal of infectious diseases.

[156]  R. Knox,et al.  “Celbenin” - resistant Staphylococci , 1961 .

[157]  R. Arbeit,et al.  Epidemiologic and clinical utility of typing systems for differentiating among strains of methicillin-resistant Staphylococcus aureus. , 1991 .