Advertisement
Mayo Clinic Proceedings Home

Stethoscopes and Health Care–Associated Infection

  • Dennis G. Maki
    Correspondence
    Correspondence: Address to Dennis G. Maki, MD, Divisions of Infectious Disease and Pulmonary/Critical Care Medicine, Department of Medicine, University of Wisconsin School of Medicine and Public Health, 5227 UWMF Centennial Building, 1685 Highland Avenue, Madison, WI 53705-2281.
    Affiliations
    Divisions of Infectious Disease and Pulmonary/Critical Care Medicine, Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI
    Search for articles by this author
      Over the past 30 years we have come to fully appreciate the enormous potential for person-to-person spread of virulent nosocomial pathogens (eg, methicillin-resistant Staphylococcus aureus [MRSA], vancomycin-resistant enterococcus [VRE], multidrug-resistant [MDR] gram-negative bacilli and Clostridium difficile, viruses such as influenza A, respiratory syncytial virus, and norovirus, and even Candida species) in the health care setting, with devastating infection being the most feared iatrogenic consequence and one of the greatest threats to hospital safety.
      • Maki D.G.
      • Tsigrelis C.
      Nosocomial infection in the intensive care unit.
      • Rosenthal V.D.
      • Bijie H.
      • Maki D.G.
      • et al.
      International Nosocomial Infection Control Consortium (INICC) report, data summary of 36 countries, for 2004-2009.
      It has long been accepted that the major reservoir of nosocomial infection is infected or colonized patients and the major mode of transmission is the transient carriage of nosocomial pathogens on the hands of noncolonized health care workers having direct physical contact with patients.
      • Maki D.G.
      Control of colonization and transmission of pathogenic bacteria in the hospital.
      Hand hygiene before and after direct patient contact—now most often with a waterless alcohol gel or hand rub—has become an uncompromising expectation for modern-day health care workers.
      • Boyce J.M.
      • Pittet D.
      Healthcare Infection Control Practices Advisory CommitteeHICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force
      Guideline for Hand Hygiene in Healthcare Settings: Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HIPAC/SHEA/APIC/IDSA Hand Hygiene Task Force.
      Although it had long been held that microorganisms in the inanimate hospital environment do not play a significant role in the acquisition of nosocomial infection,
      • Maki D.G.
      • Alvarado C.J.
      • Hassemer C.A.
      • Zilz M.A.
      Relation of the inanimate hospital environment to endemic nosocomial infection.
      it has become evident in recent years that surfaces in hospitals touched by patients or health care workers readily become contaminated by “environmental pathogens,” such as MRSA, VRE, Acinetobacter baumanii, C difficile, respiratory syncytial virus, and norovirus, which collectively have a unique capacity to survive dessiccation in a viable, transmissible form for days to months. Compelling epidemiologic data indicate that contamination of inanimate surfaces in hospitals is an important reservoir of these pathogens and has driven a move toward more comprehensive surface decontamination with bleach solutions, ultraviolet light, or aerosolization of hydrogen peroxide or peroxacetic acid.
      • Weber D.J.
      • Rutala W.A.
      • Miller M.B.
      • Huslage K.
      • Sickbert-Bennett E.
      Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species.
      Auscultation of the heart, lungs, abdomen, and major arteries with a stethoscope has long been considered an integral part of the physical examination, and most health care providers prefer to use their own stethoscope. It has long been known that the diaphragms and bells of stethoscopes randomly sampled in a health care setting, such as a hospital, are almost universally contaminated by potential nosocomial pathogens,
      • Jones J.S.
      • Hoerle D.
      • Riekse R.
      Stethoscopes: a potential vector of infection?.
      • Marinella M.A.
      • Pierson C.
      • Chenoweth C.
      The stethoscope. A potential source of nosocomial infection?.
      • Bernard L.
      • Kereveur A.
      • Durand D.
      • et al.
      Bacterial contamination of hospital physicians’ stethoscopes.
      • Zachary K.C.
      • Bayne P.S.
      • Morrison V.J.
      • Ford D.S.
      • Silver L.C.
      • Hooper D.C.
      Contamination of gowns, gloves, and stethoscopes with vancomycin-resistant enterococci.
      • Parmar R.C.
      • Valvi C.C.
      • Sira P.
      • Kamat J.R.
      A prospective, randomised, double-blind study of comparative efficacy of immediate versus daily cleaning of stethoscope using 66% ethyl alcohol.
      • Bandi S.
      • Uddin L.
      • Milward K.
      • Aliyu S.
      • Makwana N.
      How clean are our stethoscopes and do we need to clean them?.
      • Fenelon L.
      • Holcroft L.
      • Waters N.
      Contamination of stethoscopes with MRSA and current disinfection practices.
      • Uneke C.J.
      • Ogbonna A.
      • Oyibo P.G.
      • Ekuma U.
      Bacteriological assessment of stethoscopes used by medical students in Nigeria: implications for nosocomial infection control.
      • Schroeder A.
      • Schroeder M.A.
      • D’Amico F.
      What’s growing on your stethoscope? (And what you can do about it).
      • Uneke C.J.
      • Ogbonna A.
      • Oyibo P.G.
      • Onu C.M.
      Bacterial contamination of stethoscopes used by health workers: public health implications.
      • Vajravelu R.K.
      • Guerrero D.M.
      • Jury L.A.
      • Donskey C.J.
      Evaluation of stethoscopes as vectors of Clostridium difficile and methicillin-resistant Staphylococcus aureus.
      • Merlin M.A.
      • Wong M.L.
      • Pryor P.W.
      • et al.
      Prevalence of methicillin-resistant Staphylococcus aureus on the stethoscopes of emergency medical services providers.
      most often staphylococci—MRSA up to 32% of the time
      • Merlin M.A.
      • Wong M.L.
      • Pryor P.W.
      • et al.
      Prevalence of methicillin-resistant Staphylococcus aureus on the stethoscopes of emergency medical services providers.
      —but also C difficile,
      • Vajravelu R.K.
      • Guerrero D.M.
      • Jury L.A.
      • Donskey C.J.
      Evaluation of stethoscopes as vectors of Clostridium difficile and methicillin-resistant Staphylococcus aureus.
      resistant gram-negative bacilli, and even viruses,
      • Blydt-Hansen T.
      • Subbarao K.
      • Quennec P.
      • McDonald J.
      Recovery of respiratory syncytial virus from stethoscopes by conventional viral culture and polymerase chain reaction.
      and studies have shown that stethoscope contamination by these microorganisms is commonly acquired from colonized or infected patients.
      • Bernard L.
      • Kereveur A.
      • Durand D.
      • et al.
      Bacterial contamination of hospital physicians’ stethoscopes.
      • Zachary K.C.
      • Bayne P.S.
      • Morrison V.J.
      • Ford D.S.
      • Silver L.C.
      • Hooper D.C.
      Contamination of gowns, gloves, and stethoscopes with vancomycin-resistant enterococci.
      In this issue of Mayo Clinic Proceedings, Longtin et al
      • Longtin Y.
      • Schneider A.
      • Tschopp A.
      • et al.
      Contamination of stethoscopes and physicians’ hands following a physical examination.
      report an innovative study of ungloved physicians who auscultated MRSA-colonized patients with presterilized stethoscopes, showing that the fingertips of the examiners or the diaphragms of their stethoscopes acquired MRSA contamination during 76% of the examinations. They found a powerful correlation between counts on examiners’ hands and the quantitative level of contamination of the stethoscope with each examination, both for total bacterial counts and for MRSA. The efficiency of transmission of MRSA from the trunk of colonized or infected patients to the hands of health care workers and their stethoscopes rigorously documented in this unique real-life study is almost staggering. One can ask, why are we all not MRSA carriers?
      Given that microorganisms on contaminated stethoscopes are readily transmitted back to the surfaces they touch
      • Jones J.S.
      • Hoerle D.
      • Riekse R.
      Stethoscopes: a potential vector of infection?.
      • Bernard L.
      • Kereveur A.
      • Durand D.
      • et al.
      Bacterial contamination of hospital physicians’ stethoscopes.
      • Zachary K.C.
      • Bayne P.S.
      • Morrison V.J.
      • Ford D.S.
      • Silver L.C.
      • Hooper D.C.
      Contamination of gowns, gloves, and stethoscopes with vancomycin-resistant enterococci.
      • Bandi S.
      • Uddin L.
      • Milward K.
      • Aliyu S.
      • Makwana N.
      How clean are our stethoscopes and do we need to clean them?.
      • Uneke C.J.
      • Ogbonna A.
      • Oyibo P.G.
      • Ekuma U.
      Bacteriological assessment of stethoscopes used by medical students in Nigeria: implications for nosocomial infection control.
      and must be considered a preventable source of nosocomial colonization (and subsequent nosocomial infection) of patients, this mode of transmission would seem no less important than the uncleansed hands of health care workers. Although a number of studies have microbiologically and epidemiologically implicated electronic thermometers in the genesis of nosocomial outbreaks,
      • Livornese Jr., L.L.
      • Dias S.
      • Samel C.
      • et al.
      Hospital-acquired infection with vancomycin-resistant Enterococcus faecium transmitted by electronic thermometers.
      • van den Berg R.W.
      • Claahsen H.L.
      • Niessen M.
      • Muytjens H.L.
      • Liem K.
      • Voss A.
      Enterobacter cloacae outbreak in the NICU related to disinfected thermometers.
      • Dijk Y.
      • Bik E.M.
      • Hochstenbach-Vernooij S.
      • et al.
      Management of an outbreak of Enterobacter cloacae in a neonatal unit using simple preventive measures.
      only a single report has linked the contamination of stethoscopes to infections in patients in an outbreak in a neonatal intensive care unit (ICU) epidemiologically as well as microbiologically
      • Hoşbul T.
      • Ozyurt M.
      • Karademir F.
      • Süleymanoğlu S.
      • Haznedaroğlu T.
      Investigation of a nosocomial outbreak caused by ESBL positive Klebsiella pneumoniae in neonatal intensive care unit by AP-PCR.
      and no published study has made an unequivocal association with endemic health care–associated infections. However, if hand hygiene is considered an essential infection control measure to help prevent the spread of pathogens both in the health care setting and in the community,
      • Boyce J.M.
      • Pittet D.
      Healthcare Infection Control Practices Advisory CommitteeHICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force
      Guideline for Hand Hygiene in Healthcare Settings: Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HIPAC/SHEA/APIC/IDSA Hand Hygiene Task Force.
      it seems only logical that measures to minimize the accumulation of potential nosocomial pathogens on stethoscopes are needed to prevent transmission to vulnerable patients.
      Studies have shown that wiping the head of a stethoscope with a 70% alcohol pledget
      • Jones J.S.
      • Hoerle D.
      • Riekse R.
      Stethoscopes: a potential vector of infection?.
      • Marinella M.A.
      • Pierson C.
      • Chenoweth C.
      The stethoscope. A potential source of nosocomial infection?.
      • Bernard L.
      • Kereveur A.
      • Durand D.
      • et al.
      Bacterial contamination of hospital physicians’ stethoscopes.
      • Zachary K.C.
      • Bayne P.S.
      • Morrison V.J.
      • Ford D.S.
      • Silver L.C.
      • Hooper D.C.
      Contamination of gowns, gloves, and stethoscopes with vancomycin-resistant enterococci.
      • Parmar R.C.
      • Valvi C.C.
      • Sira P.
      • Kamat J.R.
      A prospective, randomised, double-blind study of comparative efficacy of immediate versus daily cleaning of stethoscope using 66% ethyl alcohol.
      • Bandi S.
      • Uddin L.
      • Milward K.
      • Aliyu S.
      • Makwana N.
      How clean are our stethoscopes and do we need to clean them?.
      • Fenelon L.
      • Holcroft L.
      • Waters N.
      Contamination of stethoscopes with MRSA and current disinfection practices.
      • Vajravelu R.K.
      • Guerrero D.M.
      • Jury L.A.
      • Donskey C.J.
      Evaluation of stethoscopes as vectors of Clostridium difficile and methicillin-resistant Staphylococcus aureus.
      or wiping it with the antiseptic used for hand hygiene
      • Jones J.S.
      • Hoerle D.
      • Riekse R.
      Stethoscopes: a potential vector of infection?.
      • Marinella M.A.
      • Pierson C.
      • Chenoweth C.
      The stethoscope. A potential source of nosocomial infection?.
      • Bernard L.
      • Kereveur A.
      • Durand D.
      • et al.
      Bacterial contamination of hospital physicians’ stethoscopes.
      • Uneke C.J.
      • Ogbonna A.
      • Oyibo P.G.
      • Onu C.M.
      Bacterial contamination of stethoscopes used by health workers: public health implications.
      or a hospital surface disinfectant
      • Jones J.S.
      • Hoerle D.
      • Riekse R.
      Stethoscopes: a potential vector of infection?.
      • Marinella M.A.
      • Pierson C.
      • Chenoweth C.
      The stethoscope. A potential source of nosocomial infection?.
      • Bernard L.
      • Kereveur A.
      • Durand D.
      • et al.
      Bacterial contamination of hospital physicians’ stethoscopes.
      greatly reduces—usually eliminates—the bioburden of aerobic bacterial contamination. Moreover, the personal stethoscopes of health care workers who practice regular decontamination have been found to be less likely to be contaminated by MRSA and other MDR pathogens.
      • Parmar R.C.
      • Valvi C.C.
      • Sira P.
      • Kamat J.R.
      A prospective, randomised, double-blind study of comparative efficacy of immediate versus daily cleaning of stethoscope using 66% ethyl alcohol.
      • Bandi S.
      • Uddin L.
      • Milward K.
      • Aliyu S.
      • Makwana N.
      How clean are our stethoscopes and do we need to clean them?.
      • Fenelon L.
      • Holcroft L.
      • Waters N.
      Contamination of stethoscopes with MRSA and current disinfection practices.
      • Uneke C.J.
      • Ogbonna A.
      • Oyibo P.G.
      • Ekuma U.
      Bacteriological assessment of stethoscopes used by medical students in Nigeria: implications for nosocomial infection control.
      • Uneke C.J.
      • Ogbonna A.
      • Oyibo P.G.
      • Onu C.M.
      Bacterial contamination of stethoscopes used by health workers: public health implications.
      As such, health care workers should be expected to routinely decontaminate the head of their personal stethoscope between patients, logically when they do postexamination hand hygiene.
      Unfortunately, the efficacy of these simple approaches to on-site decontamination of stethoscopes for removing C difficile spores or viruses that can also be present is unknown. It has long been accepted that dedicated stethoscopes—used only on the isolated patient and sent to Central Supply for decontamination with ethylene oxide gas when the patient is transferred or discharged—are an integral feature of barrier isolation to prevent the spread of microorganisms known to be spread by direct physical contact, such as MRSA, VRE, MDR gram-negative bacilli, and C difficile but also all the respiratory and enteric viruses, and enteric parasites such as Giardia lamblia and Cryptosporidium species.
      • Siegel J.D.
      • Rhinehart E.
      • Jackson M.
      • Chiarello L.
      Health Care Infection Control Practices Advisory Committee
      2007 Guideline for Isolation Precautions: Preventing Transmission of Infectious Agents in Health Care Settings.
      However, it has also become clear that for every patient known to be colonized or infected by an MDR nosocomial pathogen because of a positive clinical culture or C difficile polymerase chain reaction test, there are many more patients on that same patient care unit with undetected colonization—patients who pose a greater risk of spreading these microorganisms than patients known to be colonized or infected and in isolation.
      • Safdar N.
      • Maki D.G.
      The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, enterococcus, gram-negative bacilli, Clostridium difficile, and Candida.
      This fact has formed the basis for “search and destroy” strategies for preventing MRSA and VRE infection, screening newly admitted patients for carriage to determine the need for barrier isolation and decolonization,
      • Vos M.C.
      • Behrendt M.D.
      • Melles D.C.
      • et al.
      5 years of experience implementing a methicillin-resistant Staphylococcus aureus search and destroy policy at the largest university medical center in the Netherlands.
      • Jain R.
      • Kralovic S.M.
      • Evans M.E.
      • et al.
      Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections.
      and most recently, putatively more cost-effective and broadly effective preventive strategies in the ICU, bypassing screening and subjecting all patients in the ICU to daily chlorhexidine bathing,
      • Bleasdale S.C.
      • Trick W.E.
      • Gonzalez I.M.
      • Lyles R.D.
      • Hayden M.K.
      • Weinstein R.A.
      Effectiveness of chlorhexidine bathing to reduce catheter-associated bloodstream infections in medical intensive care unit patients.
      • Climo M.W.
      • Yokoe D.S.
      • Warren D.K.
      • et al.
      Effect of daily chlorhexidine bathing on hospital-acquired infection.
      with or without the use of nasal mupirocin.
      • Huang S.S.
      • Septimus E.
      • Kleinman K.
      • et al.
      CDC Prevention Epicenters ProgramAHRQ DECIDE Network and Healthcare-Associated Infections Program
      Targeted versus universal decolonization to prevent ICU infection.
      Studies showing that neckties and clothing readily become contaminated by nosocomial pathogens such as MRSA or C difficile have driven a new policy in UK National Health Service hospitals forbidding neckties and jackets and mandating hospital-provided reprocessable overgarments for health care workers involved in direct patient care.
      General Health Protection, Department of HealthHealth Act 2006
      Code of Practice for the Prevention and Control of Healthcare Associated Infections. Uniforms and Workwear. An Evidence Base for Developing Local Policy.
      Notwithstanding a recent multicenter trial that showed only moderate benefit,
      • Harris A.D.
      • Pineles L.
      • Belton B.
      • et al.
      Universal glove and gown use and acquisition of antibiotic-resistant bacteria in the ICU: a randomized trial.
      preemptive barrier isolation of all high-risk patients, with dedicated stethoscopes, to prevent the spread of nosocomial pathogens has shown efficacy
      • Klein B.S.
      • Perloff W.H.
      • Maki D.G.
      Reduction of nosocomial infection during pediatric intensive care by protective isolation.
      and is practiced in many ICUs around the world.
      In sum, I believe that it is now time for the use of dedicated stethoscopes with all ICU patients and a case can be made for all hospitalized patients. The complaint that the cheap stethoscopes many hospitals purchase for isolation rooms are barely functional can be obviated by purchasing higher quality stethoscopes in bulk with a unique and garish pattern on the tubing (eg, iridescent orange or striped) to deter theft, the major impediment to hospitals purchasing more expensive, high-quality institutional stethoscopes.
      Promising advances in antiseptic surface technology to prevent surface microbial contamination
      • Karpanen T.J.
      • Casey A.L.
      • Lambert P.A.
      • et al.
      The antimicrobial efficacy of copper alloy furnishing in the clinical environment: a crossover study.
      • Bazaka K.
      • Jacob M.V.
      • Crawford R.J.
      • Ivanova E.P.
      Efficient surface modification of biomaterial to prevent biofilm formation and the attachment of microorganisms.
      may allow a return to the routine use of personal stethoscopes in the future.

      References

        • Maki D.G.
        • Tsigrelis C.
        Nosocomial infection in the intensive care unit.
        in: Parrillo J.E. Dellinger R.P. Critical Care Medicine. Principles of Diagnosis and Management. (4th ed.). Mosby, Philadelphia, PA2014: 825-869
        • Rosenthal V.D.
        • Bijie H.
        • Maki D.G.
        • et al.
        International Nosocomial Infection Control Consortium (INICC) report, data summary of 36 countries, for 2004-2009.
        Am J Infect Control. 2012; 40: 396-407
        • Maki D.G.
        Control of colonization and transmission of pathogenic bacteria in the hospital.
        Ann Intern Med. 1978; 89: 777-780
        • Boyce J.M.
        • Pittet D.
        • Healthcare Infection Control Practices Advisory Committee
        • HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force
        Guideline for Hand Hygiene in Healthcare Settings: Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HIPAC/SHEA/APIC/IDSA Hand Hygiene Task Force.
        Am J Infect Control. 2002; 30: S1-S46
        • Maki D.G.
        • Alvarado C.J.
        • Hassemer C.A.
        • Zilz M.A.
        Relation of the inanimate hospital environment to endemic nosocomial infection.
        N Engl J Med. 1982; 307: 1562-1566
        • Weber D.J.
        • Rutala W.A.
        • Miller M.B.
        • Huslage K.
        • Sickbert-Bennett E.
        Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species.
        Am J Infect Control. 2010; 38: S25-S33
        • Jones J.S.
        • Hoerle D.
        • Riekse R.
        Stethoscopes: a potential vector of infection?.
        Ann Emerg Med. 1995; 26: 296-299
        • Marinella M.A.
        • Pierson C.
        • Chenoweth C.
        The stethoscope. A potential source of nosocomial infection?.
        Arch Intern Med. 1997; 157: 786-790
        • Bernard L.
        • Kereveur A.
        • Durand D.
        • et al.
        Bacterial contamination of hospital physicians’ stethoscopes.
        Infect Control Hosp Epidemiol. 1999; 20: 626-628
        • Zachary K.C.
        • Bayne P.S.
        • Morrison V.J.
        • Ford D.S.
        • Silver L.C.
        • Hooper D.C.
        Contamination of gowns, gloves, and stethoscopes with vancomycin-resistant enterococci.
        Infect Control Hosp Epidemiol. 2001; 22: 560-564
        • Parmar R.C.
        • Valvi C.C.
        • Sira P.
        • Kamat J.R.
        A prospective, randomised, double-blind study of comparative efficacy of immediate versus daily cleaning of stethoscope using 66% ethyl alcohol.
        Indian J Med Sci. 2004; 58: 423-430
        • Bandi S.
        • Uddin L.
        • Milward K.
        • Aliyu S.
        • Makwana N.
        How clean are our stethoscopes and do we need to clean them?.
        J Infect. 2008; 57: 355-356
        • Fenelon L.
        • Holcroft L.
        • Waters N.
        Contamination of stethoscopes with MRSA and current disinfection practices.
        J Hosp Infect. 2009; 71: 376-378
        • Uneke C.J.
        • Ogbonna A.
        • Oyibo P.G.
        • Ekuma U.
        Bacteriological assessment of stethoscopes used by medical students in Nigeria: implications for nosocomial infection control.
        World Health Popul. 2008; 10: 53-61
        • Schroeder A.
        • Schroeder M.A.
        • D’Amico F.
        What’s growing on your stethoscope? (And what you can do about it).
        J Fam Pract. 2009; 58: 404-409
        • Uneke C.J.
        • Ogbonna A.
        • Oyibo P.G.
        • Onu C.M.
        Bacterial contamination of stethoscopes used by health workers: public health implications.
        J Infect Dev Ctries. 2010; 4: 436-441
        • Vajravelu R.K.
        • Guerrero D.M.
        • Jury L.A.
        • Donskey C.J.
        Evaluation of stethoscopes as vectors of Clostridium difficile and methicillin-resistant Staphylococcus aureus.
        Infect Control Hosp Epidemiol. 2012; 33: 96-98
        • Merlin M.A.
        • Wong M.L.
        • Pryor P.W.
        • et al.
        Prevalence of methicillin-resistant Staphylococcus aureus on the stethoscopes of emergency medical services providers.
        Prehosp Emerg Care. 2009; 13: 71-74
        • Blydt-Hansen T.
        • Subbarao K.
        • Quennec P.
        • McDonald J.
        Recovery of respiratory syncytial virus from stethoscopes by conventional viral culture and polymerase chain reaction.
        Pediatr Infect Dis J. 1999; 18: 164-165
        • Longtin Y.
        • Schneider A.
        • Tschopp A.
        • et al.
        Contamination of stethoscopes and physicians’ hands following a physical examination.
        Mayo Clin Proc. 2014; 89: 291-299
        • Livornese Jr., L.L.
        • Dias S.
        • Samel C.
        • et al.
        Hospital-acquired infection with vancomycin-resistant Enterococcus faecium transmitted by electronic thermometers.
        Ann Intern Med. 1992; 117: 112-116
        • van den Berg R.W.
        • Claahsen H.L.
        • Niessen M.
        • Muytjens H.L.
        • Liem K.
        • Voss A.
        Enterobacter cloacae outbreak in the NICU related to disinfected thermometers.
        Hosp Infect. 2000; 45: 29-34
        • Dijk Y.
        • Bik E.M.
        • Hochstenbach-Vernooij S.
        • et al.
        Management of an outbreak of Enterobacter cloacae in a neonatal unit using simple preventive measures.
        J Hosp Infect. 2002; 51: 21-26
        • Hoşbul T.
        • Ozyurt M.
        • Karademir F.
        • Süleymanoğlu S.
        • Haznedaroğlu T.
        Investigation of a nosocomial outbreak caused by ESBL positive Klebsiella pneumoniae in neonatal intensive care unit by AP-PCR.
        Mikrobiyol Bul. 2012; 46: 101-105
        • Siegel J.D.
        • Rhinehart E.
        • Jackson M.
        • Chiarello L.
        • Health Care Infection Control Practices Advisory Committee
        2007 Guideline for Isolation Precautions: Preventing Transmission of Infectious Agents in Health Care Settings.
        Am J Infect Control. 2007; 35: S65-S164
        • Safdar N.
        • Maki D.G.
        The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, enterococcus, gram-negative bacilli, Clostridium difficile, and Candida.
        Ann Intern Med. 2002; 136: 834-844
        • Vos M.C.
        • Behrendt M.D.
        • Melles D.C.
        • et al.
        5 years of experience implementing a methicillin-resistant Staphylococcus aureus search and destroy policy at the largest university medical center in the Netherlands.
        Infect Control Hosp Epidemiol. 2009; 30: 977-984
        • Jain R.
        • Kralovic S.M.
        • Evans M.E.
        • et al.
        Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections.
        N Engl J Med. 2011; 364: 1419-1430
        • Bleasdale S.C.
        • Trick W.E.
        • Gonzalez I.M.
        • Lyles R.D.
        • Hayden M.K.
        • Weinstein R.A.
        Effectiveness of chlorhexidine bathing to reduce catheter-associated bloodstream infections in medical intensive care unit patients.
        Arch Intern Med. 2007; 167: 2073-2079
        • Climo M.W.
        • Yokoe D.S.
        • Warren D.K.
        • et al.
        Effect of daily chlorhexidine bathing on hospital-acquired infection.
        N Engl J Med. 2013; 368: 533-542
        • Huang S.S.
        • Septimus E.
        • Kleinman K.
        • et al.
        • CDC Prevention Epicenters Program
        • AHRQ DECIDE Network and Healthcare-Associated Infections Program
        Targeted versus universal decolonization to prevent ICU infection.
        N Engl J Med. 2013; 368: 2255-2265
        • General Health Protection, Department of Health
        • Health Act 2006
        Code of Practice for the Prevention and Control of Healthcare Associated Infections. Uniforms and Workwear. An Evidence Base for Developing Local Policy.
        Department of Health, London2006
        • Harris A.D.
        • Pineles L.
        • Belton B.
        • et al.
        Universal glove and gown use and acquisition of antibiotic-resistant bacteria in the ICU: a randomized trial.
        JAMA. 2013; 310: 1571-1580
        • Klein B.S.
        • Perloff W.H.
        • Maki D.G.
        Reduction of nosocomial infection during pediatric intensive care by protective isolation.
        N Engl J Med. 1989; 320: 1714-1721
        • Karpanen T.J.
        • Casey A.L.
        • Lambert P.A.
        • et al.
        The antimicrobial efficacy of copper alloy furnishing in the clinical environment: a crossover study.
        Infect Control Hosp Epidemiol. 2012; 33: 3-9
        • Bazaka K.
        • Jacob M.V.
        • Crawford R.J.
        • Ivanova E.P.
        Efficient surface modification of biomaterial to prevent biofilm formation and the attachment of microorganisms.
        Appl Microbiol Biotechnol. 2012; 95: 299-311

      Linked Article