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What can we learn from each other in infection control? Experience in Europe compared with the USA

  • S. Harbarth
    Correspondence
    Address: Infection Control Programme, Department of Internal Medicine, University of Geneva Hospitals, 1211 Geneva 14, Switzerland. Tel.: +41 22 372 98 28; fax: +41 22 372 39 87.
    Affiliations
    Infection Control Programme, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
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Published:February 04, 2013DOI:https://doi.org/10.1016/j.jhin.2012.12.003

      Summary

      Infection control practices in Europe and the USA have been influenced and shaped over the last 50 years by various technological developments, historical experiences and research schools that have led to different approaches to the control and prevention of healthcare-associated infections. This narrative review attempts to answer the question: Which are the most useful lessons to be learned from this historical experience, as well as methods and measures advocated on both sides of the Atlantic, in order to determine best practices to control and prevent healthcare-associated infections and antimicrobial resistance? The review is intended neither as an expansion of ongoing debates on controversial scientific issues, nor as a complete historical review of modern hospital epidemiology, but should be considered rather a personal viewpoint that tries to bridge the gap between US-influenced hospital epidemiology and traditional microbiology-based hygiene in Europe.

      Keywords

      Introduction

      Healthcare-associated infections (HCAIs) have become a worldwide problem.
      • Kock R.
      • Becker K.
      • Cookson B.
      • et al.
      Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe.
      • Allegranzi B.
      • Bagheri Nejad S.
      • Combescure C.
      • et al.
      Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis.
      Yet the reasons for the uneven geographic distribution of HCAI rates are not fully understood. For instance, there are important differences in the epidemiology of HCAIs and multidrug-resistant organisms (MDROs) between the USA and Europe.
      • Goossens H.
      Spread of vancomycin-resistant enterococci: differences between the United States and Europe.
      • Harbarth S.
      • Albrich W.
      • Goldmann D.A.
      • Huebner J.
      Control of multiply resistant cocci: do international comparisons help?.
      Disparities may be explained by several determinants: (i) surveillance methods, including diagnostic practices and laboratory recognition; (ii) infection control knowledge and practices; (iii) antibiotic prescribing practices; (iv) hospital characteristics and patient case-mix; (v) cultural factors (e.g. hygiene behaviour); (vi) factors related to healthcare systems and associated quality standards; (vii) available resources dedicated to hospital hygiene; (viii) legal constraints; (ix) political commitment.
      • Harbarth S.
      • Albrich W.
      • Goldmann D.A.
      • Huebner J.
      Control of multiply resistant cocci: do international comparisons help?.
      • Harbarth S.
      • Samore M.H.
      Antimicrobial resistance determinants and future control.
      • Borg M.A.
      Could the incidence of healthcare infections in Europe simply be a reflection of overall quality standards?.
      Certainly, effects exerted at the macro level by the healthcare system and political environment contribute substantially to the observed differences in HCAI rates.
      • Pittet D.
      Infection control and quality health care in the new millennium.
      • Marcel J.P.
      • Alfa M.
      • Baquero F.
      • et al.
      Healthcare-associated infections: think globally, act locally.
      But even more importantly, HCAI control practices in Europe and the USA have been influenced and shaped over the last 50 years by various technological developments, historical experiences and research schools that lead to different approaches to the control and prevention of HCAI.
      • Goldmann D.A.
      Nosocomial infection control in the United States of America.
      In particular, there is still ongoing controversy among European hospital hygienists (especially in Germany and Eastern Europe) about the benefits and limitations of epidemiological and patient outcome-centred methods for the prevention and control of HCAIs, since traditional microbiology-based approaches and ‘holistic’ strategies to hospital hygiene have until the 1990s dominated the field in Europe.
      • Harbarth S.
      Epidemiologic methods for the prevention of nosocomial infections.
      • Exner M.
      • Hartemann P.
      • Kistemann T.
      Hygiene and health – the need for a holistic approach.
      Therefore, the question arises: Which are the most useful lessons to be learned from this historical experience, as well as methods and measures advocated on both sides of the Atlantic, in order to determine best practices to control and prevent HCAIs and MDROs? The overview presented here is intended neither as an expansion of ongoing debates on controversial scientific issues such as MDRO screening and isolation practices, nor as a complete historical review of modern hospital epidemiology, but should be considered rather a personal viewpoint that tries to bridge the gap between US-influenced hospital epidemiology and microbiology-based hygiene in Europe.
      • Harbarth S.
      • Hawkey P.M.
      • Tenover F.
      • Stefani S.
      • Pantosti A.
      • Struelens M.J.
      Update on screening and clinical diagnosis of meticillin-resistant Staphylococcus aureus (MRSA).
      • Kluytmans J.
      • Harbarth S.
      Control of MRSA in intensive care units.

      Useful lessons from the USA

      Role of epidemiological methods and surveillance

      Although many of the basic ideas of healthcare epidemiology can be traced back to Semmelweis, the formal application of epidemiological methods in infection control received a substantial boost only 100 years later during the 1970s and 1980s, with the publication of a number of methodologically oriented articles from US colleagues that brought innovation to the field.
      • Pittet D.
      • Boyce J.M.
      Hand hygiene and patient care: pursuing the Semmelweis legacy.
      • Harbarth S.
      • Albrich W.
      • Pittet D.
      Semmelweis' legacy: insights from an international survey among 265,000 students in 32 countries.
      • Freeman J.
      • Goldmann D.A.
      • McGowan Jr., J.E.
      Confounding and the analysis of multiple variables in hospital epidemiology.
      • Freeman J.
      • Goldmann D.A.
      • McGowan J.E.
      Methodologic issues in hospital epidemiology. IV. Risk ratios, confounding, effect modification, and the analysis of multiple variables.
      Based on the assumption that HCAIs have causal and preventive factors that can be identified through systematic investigation, these studies demonstrated convincingly that epidemiological methods add important knowledge to reduce the risk and rates of HCAIs.
      • Harbarth S.
      Epidemiologic methods for the prevention of nosocomial infections.
      Thus, the conceptual framework was laid for many interventional and observational studies in the field. Since these early pioneering times of modern hospital epidemiology, many investigators and studies have demonstrated the explanatory power of descriptive, analytical and experimental epidemiology in our field.
      • Eggimann P.
      • Harbarth S.
      • Ricou B.
      • et al.
      Acute respiratory distress syndrome after bacteremic sepsis does not increase mortality.
      • Zawacki A.
      • O'Rourke E.
      • Potter-Bynoe G.
      • Macone A.
      • Harbarth S.
      • Goldmann D.
      An outbreak of Pseudomonas aeruginosa pneumonia and bloodstream infection associated with intermittent otitis externa in a healthcare worker.
      • Fischer J.E.
      • Harbarth S.
      • Agthe A.G.
      • et al.
      Quantifying uncertainty: physicians' estimates of infection in critically ill neonates and children.
      • Samore M.H.
      • Venkataraman L.
      • Degirolami P.C.
      • et al.
      Genotypic and phenotypic analysis of Clostridium difficile correlated with previous antibiotic exposure.
      • Graves N.
      • Harbarth S.
      • Beyersmann J.
      • Barnett A.
      • Halton K.
      • Cooper B.
      Estimating the cost of health care-associated infections: mind your p's and q's.
      Furthermore, advanced biostatistical tools such as process control charts have been introduced to better detect clusters of infections or other unusual in-hospital adverse events, and to evaluate the impact of interventions to prevent HCAIs (Figure 1).
      • Quesenberry C.P.
      Statistical process control geometric Q-chart for nosocomial infection surveillance.
      • Harbarth S.
      • Fankhauser C.
      • Schrenzel J.
      • et al.
      Universal screening for methicillin-resistant Staphylococcus aureus at hospital admission and nosocomial infection in surgical patients.
      Figure thumbnail gr1
      Figure 1Neonatal nursery and intensive care unit, Children's Hospital Boston (MA, USA). Incidence density of patients with nosocomial enteric Gram-negative rods resistant to third-generation cephalosporins; January 1996 to March 2001. LCL, lower control limit; CL, control limit; UWL, upper warning limit; UCL, upper control limit.
      Several landmark studies from the USA have shown that accurate diagnostic and surveillance methods are essential for designing and organizing interventions to prevent HCAIs.
      • Goldmann D.A.
      • Dixon R.E.
      • Fulkerson C.C.
      • Maki D.G.
      • Martin S.M.
      • Bennett J.V.
      The role of nationwide nosocomial infection surveillance in detecting epidemic bacteremia due to contaminated intravenous fluids.
      • Haley R.W.
      • Culver D.H.
      • Morgan W.M.
      • White J.W.
      • Emori T.G.
      • Hooton T.M.
      Increased recognition of infectious diseases in US hospitals through increased use of diagnostic tests, 1970–1976.
      In response to questions raised about the efficacy of the methods adopted in hospital epidemiological practice, several studies attributed a decrease in nosocomial infections to effective HCAI control programmes.
      • Shoji K.T.
      • Axnick K.
      • Rytel M.W.
      Infections and antibiotic use in a large municipal hospital 1970–1972: a prospective analysis of the effectiveness of a continuous surveillance program.
      • Cruse P.J.E.
      • Foord R.
      The epidemiology of wound infection. A 10-year prospective study of 62,939 wounds.
      These were followed by the Centers for Disease Control and Prevention (CDC) Study on the Efficacy of Nosocomial Infection Control (SENIC) in the late 1970s, which affirmed this association in a controlled, nationwide study.
      • Haley R.W.
      • Quade D.
      • Freeman H.E.
      • Bennett J.V.
      Study on the Efficacy of Nosocomial Infection Control (SENIC Project). Summary of study design.
      • Haley R.W.
      • Culver D.H.
      • White J.W.
      The efficacy of infection surveillance and control programs in preventing nosocomial infections in U.S. hospitals.
      SENIC demonstrated an overall 32% reduction in HCAI rates associated with specific surveillance and infection control components; the reduction effect varied, however, for the different HCAI subtypes (Figure 2). Financial incentives for hospital administrators to adopt effective and patient-centred HCAI control programmes became apparent.
      • Haley R.W.
      • White J.W.
      • Culver D.H.
      • Hughes J.M.
      The financial incentive for hospitals to prevent nosocomial infections under the prospective payment system. An empirical determination from a nationally representative sample.
      Figure thumbnail gr2
      Figure 2Impact of the Centers for Disease Control and Prevention (CDC) Study on the Efficacy of Nosocomial Infection Control (SENIC) that demonstrated an overall 32% reduction in HCAI rates associated with specific surveillance and infection control components (white bars), compared with control hospitals (grey bars).
      • Haley R.W.
      • Quade D.
      • Freeman H.E.
      • Bennett J.V.
      Study on the Efficacy of Nosocomial Infection Control (SENIC Project). Summary of study design.
      • Haley R.W.
      • Culver D.H.
      • White J.W.
      The efficacy of infection surveillance and control programs in preventing nosocomial infections in U.S. hospitals.
      LRTI, lower respiratory tract infection; SSI, surgical site infection; UTI, urinary tract infection; BSI, bloodstream infection. Reproduced from Haley et al.
      • Haley R.W.
      • Culver D.H.
      • White J.W.
      The efficacy of infection surveillance and control programs in preventing nosocomial infections in U.S. hospitals.

      Evidence-based infection control and practice guidelines

      In the early 1970s, the focus of hospital hygiene in the USA shifted from environmental control (e.g. waste management) to more evidence-based, patient-centred approaches. Routine environmental sampling was discarded as a wasteful and unproductive practice.
      • Maki D.G.
      • Alvarado C.J.
      • Hassemer C.A.
      • Zilz M.A.
      Relation of the inanimate hospital environment to endemic nosocomial infection.
      During the following decades, US HCAI surveillance and control programmes focused primarily on infection in patients and, in a more limited manner, healthcare workers. Investigations in the field of HCAI control have expanded to include the prevention of device-associated infections, recognition of new opportunistic infections in immunocompromised patients and control of antimicrobial resistance through antibiotic stewardship.
      • Orth B.
      • Frei R.
      • Itin P.H.
      • et al.
      Outbreak of invasive mycoses caused by Paecilomyces lilacinus from a contaminated skin lotion.
      • Juan-Torres A.
      • Harbarth S.
      Prevention of primary bacteraemia.
      • Pagani L.
      • Gyssens I.C.
      • Huttner B.
      • Nathwani D.
      • Harbarth S.
      Navigating the web in search of resources on antimicrobial stewardship in health care institutions.
      Substantial research efforts have accompanied these developments and changes in HCAI control strategies.
      The Research Committee of the Society of Healthcare Epidemiology of America
      Enhancing patient safety by reducing healthcare-associated infections: the role of discovery and dissemination.
      Based on robust study design and large sample size, high-quality clinical studies conducted in the US have refuted the claims in favour of the routine application of preventive measures that had already been implemented and marketed in Europe, without solid proof of their efficacy, as shown recently with gentamicin–collagen sponges for infection prevention in cardiac and colorectal surgery.
      • Bennett-Guerrero E.
      • Pappas T.N.
      • Koltun W.A.
      • et al.
      Gentamicin–collagen sponge for infection prophylaxis in colorectal surgery.
      • Bennett-Guerrero E.
      • Ferguson Jr., T.B.
      • Lin M.
      • et al.
      Effect of an implantable gentamicin-collagen sponge on sternal wound infections following cardiac surgery: a randomized trial.
      Infection control in the USA has one of the longest, best documented and probably most successful histories in the preparation, dissemination and acceptance of guidelines for preventive practices under routine clinical conditions.
      • Yokoe D.S.
      • Mermel L.A.
      • Anderson D.J.
      • et al.
      A compendium of strategies to prevent healthcare-associated infections in acute care hospitals.
      Beginning in the late 1960s, many guidelines for infection control in various healthcare settings were released by the American Hospital Association's Advisory Committee on Infections in Hospitals, the CDC and professional societies, such as the Infectious Diseases Society of America (IDSA) and the Society for Healthcare Epidemiology of America (SHEA). Other organizations and medical societies with significant activity in areas relevant to infection control guidelines also contributed and helped to develop and disseminate specific HCAI control recommendations.

      Limitations to evidence-based infection control

      It must be highlighted that many practices in infection prevention and control of MDROs have not been validated by controlled clinical trials. Unfortunately, there are many important questions in infection control for which we may never obtain data from randomized trials because of limitations in funding, lack of feasibility, and ethical dilemmas.
      • Samore M.H.
      • Harbarth S.
      A methodologically focused review of the literature in hospital epidemiology and infection control.
      Much of what has been recommended for infection control interventions over the past two decades is still based on experience, empiricism, and common sense.
      The Research Committee of the Society of Healthcare Epidemiology of America
      Enhancing patient safety by reducing healthcare-associated infections: the role of discovery and dissemination.
      Clearly, there are limitations to evidence-based infection control. If important preventive measures and clinical decisions could be made only on the basis of high-quality level 1 evidence, infection control nurses and hospital hygienists would be paralysed and not all patients could be adequately protected throughout their hospital stay.
      • Deresinski S.
      Guiding clinical care through evidence-free zones.
      As an illustrative example from the USA one could cite the ‘artificial fingernail story’. In the late 1990s, it required several outbreaks in different US hospitals that linked artificial fingernails of nurses to transmission of nosocomial pathogens to patients in order to issue a recommendation by the CDC that artificial nails, tips and wraps should not be worn by staff members providing direct patient care.
      • Foca M.
      • Jakob K.
      • Whittier S.
      • et al.
      Endemic Pseudomonas aeruginosa infection in a neonatal intensive care unit.
      • Moolenaar R.L.
      • Crutcher J.M.
      • San Joaquin V.H.
      • et al.
      A prolonged outbreak of Pseudomonas aeruginosa in a neonatal intensive care unit: did staff fingernails play a role in disease transmission?.
      • Parry M.F.
      • Grant B.
      • Yukna M.
      • et al.
      Candida osteomyelitis and diskitis after spinal surgery: an outbreak that implicates artificial nail use.
      Not surprisingly, ‘requiring short natural fingernails is a reasonable policy’ even without clinical studies, a message reminding us of the famous article in the British Medical Journal's Christmas edition of 2003 stating that ‘parachutes reduce the risk of injury after gravitational challenge, but their effectiveness has not been proved with randomized controlled trials’.
      • Moolenaar R.L.
      • Crutcher J.M.
      • San Joaquin V.H.
      • et al.
      A prolonged outbreak of Pseudomonas aeruginosa in a neonatal intensive care unit: did staff fingernails play a role in disease transmission?.
      • Smith G.C.
      • Pell J.P.
      Parachute use to prevent death and major trauma related to gravitational challenge: systematic review of randomised controlled trials.
      One may argue that common sense applied together with knowledge of basic hand hygiene rules and relevant contextual information could have prevented those outbreaks by simply forbidding artificial fingernails among nurses in vulnerable patient care areas. Interestingly, in an editorial in the New England Journal of Medicine, the need for more personal accountability in hand hygiene behaviour was highlighted by well-known opinion leaders, in contrast to the long-prevailing ‘no blame’ attitude to excuse hand hygiene failures of personnel by ‘system problems’.
      • Wachter R.M.
      • Pronovost P.J.
      Balancing “no blame” with accountability in patient safety.
      These authors even suggest that chronic failure to clean hands should result in a one-week suspension from clinical practice.
      • Wachter R.M.
      • Pronovost P.J.
      Balancing “no blame” with accountability in patient safety.
      Furthermore, many existing US guidelines in the infection control and clinical infectious disease literature do not follow the highest possible methodological standards for development of guidelines, as suggested by the Cochrane review group.
      • Jadad A.R.
      • Cook D.J.
      • Jones A.
      • et al.
      Methodology and reports of systematic reviews and meta-analyses: a comparison of Cochrane reviews with articles published in paper-based journals.
      For instance, the first CDC hand hygiene guideline published in 2002, an otherwise exemplary appraisal of the evidence, did not include a detailed description of the systematic review process.
      • Boyce J.M.
      • Pittet D.
      Guideline for hand hygiene in health-care settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force.
      Two recent systematic reviews revealed that most of IDSA's prevention and treatment guidelines are based on expert opinion, non-randomized trials, and case studies.
      • Khan A.R.
      • Khan S.
      • Zimmerman V.
      • Baddour L.M.
      • Tleyjeh I.M.
      Quality and strength of evidence of the Infectious Diseases Society of America clinical practice guidelines.
      • Lee D.H.
      • Vielemeyer O.
      Analysis of overall level of evidence behind Infectious Diseases Society of America practice guidelines.
      Only about 15% of the guidelines were supported by randomized controlled trials. Nonetheless, more than 40% of the guidelines' recommendations were classified as class A, the strongest level of treatment recommendation. Overall, many US guidelines for infectious diseases and MDRO control leave uncertain the study selection criteria, data extraction process, and quality of the included studies.
      • Samore M.H.
      • Harbarth S.
      A methodologically focused review of the literature in hospital epidemiology and infection control.

      Interdisciplinary collaboration, quality improvement and innovation

      Infection control in the USA can look back at a long-lasting history of multidisciplinary team work and interdisciplinary research.
      • Watson S.R.
      • Scales D.C.
      Improving intensive care unit quality using collaborative networks.
      By contrast with Semmelweis, who was more crusader than diplomat in his attempts to convince colleagues of the clinical effectiveness of hand hygiene, the US school of hospital epidemiology traditionally emphasized the importance of leadership and interpersonal skills in order to better advocate the sound principles guiding infection control practice.
      • Stewardson A.
      • Pittet D.
      Ignac Semmelweis – celebrating a flawed pioneer of patient safety.
      Based on partnership with clinicians and administrators from various backgrounds, the modern US-trained hospital epidemiologist is able to develop intra-hospital ties, inter-hospital networks and collaborations that are crucial for interaction and discussion of sensitive issues related to suboptimal outcomes, harmful in-hospital events and costly interventions.
      • Perencevich E.N.
      • Stone P.W.
      • Wright S.B.
      • Carmeli Y.
      • Fisman D.N.
      • Cosgrove S.E.
      Raising standards while watching the bottom line: making a business case for infection control.
      • Wright S.B.
      • Ostrowsky B.
      • Fishman N.
      • Deloney V.M.
      • Mermel L.
      • Perl T.M.
      Expanding roles of healthcare epidemiology and infection control in spite of limited resources and compensation.
      This team approach facilitates not only communication and collaboration in daily life but also interdisciplinary research projects that require expertise from various topic areas, a situation frequently encountered in healthcare epidemiological research.
      The Research Committee of the Society of Healthcare Epidemiology of America
      Enhancing patient safety by reducing healthcare-associated infections: the role of discovery and dissemination.
      Table I highlights a few examples of successful interdisciplinary research areas that link innovative ideas with expertise from areas outside traditional hospital hygiene.
      Table IApplication to infection control of innovative, interdisciplinary research and work activities in the USA
      Topic areaApplicationExamplesImpact
      Information technologyNovel electronic HCAI surveillance methodsEfficient identification of post-discharge surgical site infections with the use of automated pharmacy dispensing information, administrative data, and medical record information
      • Sands K.
      • Vineyard G.
      • Livingston J.
      • Christiansen C.
      • Platt R.
      Efficient identification of postdischarge surgical site infections: use of automated pharmacy dispensing information, administrative data, and medical record information.
      Increased efficiency with rapid feedback to wards
      Quality improvement methodsReal-life implementation of best practices in infection controlMultifaceted intervention for quality improvement in a network of intensive care units
      • Scales D.C.
      • Dainty K.
      • Hales B.
      • et al.
      A multifaceted intervention for quality improvement in a network of intensive care units: a cluster randomized trial.
      Sustained reduction of adverse patient outcomes
      Behavioural sciences and qualitative researchInfection control interventions based on behavioural change strategiesPrevention of urinary tract infections through a bundle approach linked with qualitative research methods
      • Saint S.
      • Kowalski C.P.
      • Forman J.
      • et al.
      A multicenter qualitative study on preventing hospital-acquired urinary tract infection in US hospitals.
      • Saint S.
      • Olmsted R.N.
      • Fakih M.G.
      • et al.
      Translating health care-associated urinary tract infection prevention research into practice via the bladder bundle.
      Better understanding about why hospitals use or do not use a range of available preventive practices
      HCAI, healthcare-associated infection.
      Traditionally, US-based healthcare epidemiology and infection control have focused more on surveillance and less on intervention and implementation. A strong movement started in 2001 to ‘close the quality gap’ in US hospitals, with the aims of offering performance expectations, aligning payment/accountability with quality improvement, and promoting evidence-based practice.
      • Marcel J.P.
      • Alfa M.
      • Baquero F.
      • et al.
      Healthcare-associated infections: think globally, act locally.
      Due to public pressure by consumer and patient groups (Figure 3), mandatory public reporting has been set up by law in 26 states of the USA, with variable success and impact.
      • Haustein T.
      • Gastmeier P.
      • Holmes A.
      • et al.
      Use of benchmarking and public reporting for infection control in four high-income countries.
      Therefore, SHEA has developed guidelines requiring the participation of experts and the use of standard definitions and performance indicators.
      • Wong E.S.
      • Rupp M.E.
      • Mermel L.
      • et al.
      Public disclosure of healthcare-associated infections: the role of the Society for Healthcare Epidemiology of America.
      Many different bodies (e.g. Agency for Healthcare Research and Quality; Institute for Healthcare Improvement) now act in synergy and contribute to a culture of safety in the USA, relying on executive leaders, professional teams and clinical staff to: (i) engage (make the problem real, admit that harm is untenable); (ii) educate (present the evidence, identify changes needed); (iii) execute (reduce complexity, hold efficient team meetings); and (iv) evaluate (based on measurement, feedback and visibility).
      • Marcel J.P.
      • Alfa M.
      • Baquero F.
      • et al.
      Healthcare-associated infections: think globally, act locally.
      Nevertheless, public health and quality improvement initiatives in the USA remain decentralized and underfunded; hospitals are mainly private, except for a few public institutions and the Veterans Affairs hospitals, which have been able to conduct large-scale quality improvement initiatives to reduce meticillin-resistant Staphylococcus aureus (MRSA) rates.
      • Jain R.
      • Kralovic S.M.
      • Evans M.E.
      • et al.
      Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections.
      Figure thumbnail gr3
      Figure 3Screen shot of the website of the MRSA Survivors Network, a US-based patient group attempting to increase awareness about meticillin-resistant Staphylococcus aureus-related issues.
      Infection control in the USA has been more technology-driven and prone to innovation compared with many European countries. For example, electronic medical records, electronic data collection and data mining systems now provide innovative and sophisticated data sources in many US hospitals.
      The Research Committee of the Society of Healthcare Epidemiology of America
      Enhancing patient safety by reducing healthcare-associated infections: the role of discovery and dissemination.
      These technological advances facilitate adherence to isolation protocols, increase efficiency of surveillance of HCAI and antimicrobial consumption and resistance, and may help to create new approaches to the prevention of HCAI.
      • Sands K.
      • Vineyard G.
      • Livingston J.
      • Christiansen C.
      • Platt R.
      Efficient identification of postdischarge surgical site infections: use of automated pharmacy dispensing information, administrative data, and medical record information.
      • Harbarth S.
      • Harris A.D.
      • Carmeli Y.
      • Samore M.H.
      Parallel analysis of individual and aggregated data on antibiotic exposure and resistance in gram-negative bacilli.
      • Harbarth S.
      • Levine G.L.
      • Jarvis W.R.
      • Goldmann D.A.
      • Huskins W.C.
      Computerized pharmacy databases as source of data on antimicrobial prescriptions in children's hospitals.
      • Hota B.
      • Lin M.
      • Doherty J.A.
      • et al.
      Formulation of a model for automating infection surveillance: algorithmic detection of central-line associated bloodstream infection.
      They also allow the development of clinical decision support tools for antibiotic stewardship and screening algorithms of patients at high risk of carrying MDROs, and can serve as data sources for complex epidemiological simulation and modelling studies on the impact and transmission of HCAIs and MDROs.
      • McGregor J.C.
      • Weekes E.
      • Forrest G.N.
      • et al.
      Impact of a computerized clinical decision support system on reducing inappropriate antimicrobial use: a randomized controlled trial.
      • Evans R.S.
      • Wallace C.J.
      • Lloyd J.F.
      • et al.
      Rapid identification of hospitalized patients at high risk for MRSA carriage.
      • Samore M.H.
      • Shen S.
      • Greene T.
      • et al.
      A simulation-based evaluation of methods to estimate the impact of an adverse event on hospital length of stay.
      • Beyersmann J.
      • Gastmeier P.
      • Grundmann H.
      • et al.
      Transmission-associated nosocomial infections: prolongation of intensive care unit stay and risk factor analysis using multistate models.

      Useful lessons from Europe

      The second part of this review summarizes relevant experiences and important advances in infection prevention in Europe as well as useful lessons for colleagues outside continental Europe.

      Surveillance and assessment of the burden of HCAI

      During the past decade, the basic principles of hospital epidemiology, aimed at measuring the necessity and effect of strategies to prevent HCAIs, have been successfully introduced into most European countries.
      • Harbarth S.
      • Pittet D.
      Infection prevention research in Europe: recent advances and future priorities.
      Surveillance and control of HCAIs based on epidemiological concepts are now an established component in many healthcare institutions throughout Europe.
      • Haustein T.
      • Gastmeier P.
      • Holmes A.
      • et al.
      Use of benchmarking and public reporting for infection control in four high-income countries.
      • Gastmeier P.
      • Sohr D.
      • Schwab F.
      • et al.
      Ten years of KISS: the most important requirements for success.
      • Zingg W.
      • Sax H.
      • Inan C.
      • et al.
      Hospital-wide surveillance of catheter-related bloodstream infection: from the expected to the unexpected.
      Nevertheless, large regional differences remain; a survey performed in 2001 showed that infection control programmes in many European hospitals still suffer from major deficiencies in human resources and policies.
      • Struelens M.J.
      • Wagner D.
      • Bruce J.
      • et al.
      Status of infection control policies and organisation in European hospitals, 2001: the ARPAC study.
      Furthermore, there remains debate about the challenges and disadvantages associated with current surveillance methods of monitoring HCAIs, as summarized in Table II.
      • Lin M.Y.
      • Hota B.
      • Khan Y.M.
      • et al.
      Quality of traditional surveillance for public reporting of nosocomial bloodstream infection rates.
      Table IIChallenges and disadvantages associated with current surveillance methods of monitoring HCAIs
      Disadvantages and limitationsPossible solutions and comments
      May yield excessive data, labour intensive, time-consumingElectronic files and data collection, software support, and data manager included in the surveillance staff could help to reduce the workload
      ExpensiveEstimated yearly costs of HCAIs are higher than the costs of surveillance and dedicated control staff
      May miss clusters or outbreaks in non-surveyed areas or populationsEstablishing alert mechanisms (e.g. microbiology laboratory alerts)
      Overall infection rate not valid for inter-hospital comparisonFor some measurements, availability of appropriate case-mix risk adjustment systems and external comparative data can improve external benchmarking
      Collects data only for targeted patients or units – limited information about endemic rates in the entire hospitalPerformance of hospital-wide prevalence surveys could complement prospective HCAI surveillance data and help to determine high-risk patient groups
      Poor inter-rater reliability in applying standard definitions and variable implementation of case-finding strategiesStrategies that make use of existing electronic data sources for creating process and outcome measures may reduce errors
      HCAI, healthcare-associated infection.
      There has been much progress made, especially in the field of HCAI prevention, following the establishment of the European Centre for Disease Prevention and Control (ECDC, Stockholm) in 2005, although some experts have criticized its limited staffing level, laboratory facilities and regulatory power.
      • Tibayrenc M.
      A hard lesson for Europeans: the ASEAN CDC.
      Working with European researchers, expert group meetings have led to informative exchanges of knowledge and ideas.
      • Kock R.
      • Becker K.
      • Cookson B.
      • et al.
      Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe.
      • Magiorakos A.P.
      • Srinivasan A.
      • Carey R.B.
      • et al.
      Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance.
      Key components of the ECDC's activity are HCAI and MDRO surveillance, which are now well-established themes within the Centre's core agenda and budget.
      • Dettenkofer M.
      • Ammon A.
      • Astagneau P.
      • et al.
      Infection control – a European research perspective for the next decade.
      The European ‘Council Recommendation’ on patient safety, which includes control of HCAI, shows the high priority attached to this area within the political context.
      • Dettenkofer M.
      • Ammon A.
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      • et al.
      Infection control – a European research perspective for the next decade.
      Without doubt, HCAIs are associated with adverse patient outcomes.
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      Estimating attributable mortality due to nosocomial infections acquired in intensive care units.
      However, most US-based studies on the burden of HCAI have frequently ignored the time-varying nature of exposures and have amplified confounding.
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      The attributable morbidity and mortality of ventilator-associated pneumonia in the critically ill patient.
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      The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: mortality, length of stay, and hospital charges.
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      Consequently, the most frequently applied approaches (i.e. matched cohort study; linear regression analysis) tend to overestimate the excess morbidity and mortality related to HCAI compared with more suitable methods based on multistate modelling techniques that take into account the timing of in-hospital events.
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      A simulation-based evaluation of methods to estimate the impact of an adverse event on hospital length of stay.
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      Nosocomial infection, length of stay, and time-dependent bias.
      • Graves N.
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      • et al.
      The importance of good data, analysis, and interpretation for showing the economics of reducing healthcare-associated infection.
      These newer statistical methods are applied mostly in European research projects, whereas US-based research has not yet embraced this methodological breakthrough.
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      Use of multistate models to assess prolongation of intensive care unit stay due to nosocomial infection.
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      • De Angelis G.
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      • et al.
      Multistate modelling to estimate the excess length of stay associated with meticillin-resistant Staphylococcus aureus colonisation and infection in surgical patients.
      • Lambert M.L.
      • Suetens C.
      • Savey A.
      • et al.
      Clinical outcomes of health-care-associated infections and antimicrobial resistance in patients admitted to European intensive-care units: a cohort study.
      Clearly, appropriate statistical methods are important for the analysis of excess length of stay and costs associated with HCAI because informed decisions and policy developments may depend on them.
      • De Angelis G.
      • Murthy A.
      • Beyersmann J.
      • Harbarth S.
      Estimating the impact of healthcare-associated infections on length of stay and costs.
      Exaggeration of excess costs may lead to unintentional errors in the economic analysis of intervention programmes.
      • Graves N.
      • Harbarth S.
      • Beyersmann J.
      • Barnett A.
      • Halton K.
      • Cooper B.
      Estimating the cost of health care-associated infections: mind your p's and q's.

      Control of antimicrobial consumption and resistance

      During the last two decades, Europe has made substantial progress in combating MDROs and in control of antibiotic overuse.
      • Boyce J.M.
      • Cookson B.
      • Christiansen K.
      • et al.
      Meticillin-resistant Staphylococcus aureus.
      • Struelens M.J.
      • Monnet D.L.
      Prevention of methicillin-resistant Staphylococcus aureus infection: is Europe winning the fight?.
      Innovative strategies and consensus guidelines have been issued.
      • Magiorakos A.P.
      • Srinivasan A.
      • Carey R.B.
      • et al.
      Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance.
      • Carmeli Y.
      • Akova M.
      • Cornaglia G.
      • et al.
      Controlling the spread of carbapenemase-producing Gram-negatives: therapeutic approach and infection control.
      • Wernli D.
      • Haustein T.
      • Conly J.
      • Carmeli Y.
      • Kickbusch I.
      • Harbarth S.
      A call for action: the application of The International Health Regulations to the global threat of antimicrobial resistance.
      A wide array of epidemiological studies has been undertaken in European countries at national or hospital level, helping to better understand the efficiency and problems of MDRO control in Europe.
      • van de Sande-Bruinsma N.
      • Grundmann H.
      • Verloo D.
      • et al.
      Antimicrobial drug use and resistance in Europe.
      • Ammerlaan H.
      • Seifert H.
      • Harbarth S.
      • et al.
      Adequacy of antimicrobial treatment and outcome of Staphylococcus aureus bacteremia in 9 Western European countries.
      • de Kraker M.E.
      • Wolkewitz M.
      • Davey P.G.
      • et al.
      Burden of antimicrobial resistance in European hospitals: excess mortality and length of hospital stay associated with bloodstream infections due to Escherichia coli resistant to third-generation cephalosporins.
      For instance, in a multicentre study by Meyer et al. performed between 2001 and 2008 in 53 German ICUs, carbapenem use almost doubled despite no significant change in total antibiotic use.
      • Meyer E.
      • Schwab F.
      • Schroeren-Boersch B.
      • Gastmeier P.
      Dramatic increase of third-generation cephalosporin-resistant E. coli in German intensive care units: secular trends in antibiotic drug use and bacterial resistance, 2001 to 2008.
      The exponential increase of third-generation cephalosporin resistance in Escherichia coli and other Enterobacteriaceae reported in this study led to switching empirical therapy to carbapenems to treat infections, with the subsequent emergence of carbapenem-resistant Klebsiella pneumoniae, carbapenemase-producing Gram-negative pathogens and imipenem-resistant Acinetobacter baumannii. This scenario may affect many ICUs in Europe in the near future, with resistance trends and antibiotic consumption rates influenced by different factors, including ICU characteristics (medical, surgical, general), local antibiotic policies and physicians' level of education.
      • Pagani L.
      • Afshari A.
      • Harbarth S.
      Year in review 2010: critical care – infection.
      Innovative antibiotic stewardship has been a hallmark of European research activities during the last decade.
      • Horisberger T.
      • Harbarth S.
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      • Baenziger O.
      • Fischer J.E.
      G-CSF and IL-8 for early diagnosis of sepsis in neonates and critically ill children – safety and cost effectiveness of a new laboratory prediction model: study protocol of a randomized controlled trial [ISRCTN91123847].
      • Huttner B.
      • Harbarth S.
      “Antibiotics are not automatic anymore” – the French national campaign to cut antibiotic overuse.
      For instance, numerous recent publications from Europe have assessed the application of algorithms based on procalcitonin as a biomarker of bacterial infection for antibiotic stewardship. Several high-quality clinical trials investigating the diagnostic performance and clinical effectiveness of procalcitonin have been published.
      • Nobre V.
      • Harbarth S.
      • Graf J.D.
      • Rohner P.
      • Pugin J.
      Use of procalcitonin to shorten antibiotic treatment duration in septic patients: a randomized trial.
      • Schuetz P.
      • Christ-Crain M.
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      • et al.
      Effect of procalcitonin-based guidelines vs standard guidelines on antibiotic use in lower respiratory tract infections: the ProHOSP randomized controlled trial.
      • Stolz D.
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      • Eggimann P.
      • et al.
      Procalcitonin for reduced antibiotic exposure in ventilator-associated pneumonia: a randomised study.
      • Bouadma L.
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      • Tubach F.
      • et al.
      Use of procalcitonin to reduce patients' exposure to antibiotics in intensive care units (PRORATA trial): a multicentre randomised controlled trial.
      Another recent stewardship success story to report from Europe relates to changes in antibiotic treatment guidelines in the UK, related to the increase in Clostridium difficile and multi-resistant enterobacteriacae.
      • Aldeyab M.A.
      • Devine M.J.
      • Flanagan P.
      • et al.
      Multihospital outbreak of Clostridium difficile ribotype 027 infection: epidemiology and analysis of control measures.
      • Aldeyab M.A.
      • Harbarth S.
      • Vernaz N.
      • et al.
      The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings.
      • Nathwani D.
      • Sneddon J.
      • Malcolm W.
      • et al.
      Scottish Antimicrobial Prescribing Group (SAPG): development and impact of the Scottish National Antimicrobial Stewardship Programme.
      Nevertheless, Europe's antimicrobial stewardship policies remain heterogeneous; whereas there is great progress in stewardship in some countries, other countries certainly lag behind.

      Promotion of alcohol-based hand hygiene and skin disinfection

      Despite its strong leadership role in epidemiological research, the USA still trails behind most European countries with the promotion of bedside, alcohol-based, waterless hand disinfection, considered widely to be among the most important tools to prevent the spread of nosocomial MDROs.
      • Harbarth S.
      • Pittet D.
      • Grady L.
      • Goldmann D.A.
      Compliance with hand hygiene practice in pediatric intensive care.
      In Europe, large-scale hand hygiene promotion campaigns have been conducted in a majority of countries.
      • Magiorakos A.P.
      • Suetens C.
      • Boyd L.
      • et al.
      National hand hygiene campaigns in Europe, 2000–2009.
      In the USA, the misconception that sink-based hand washing with antimicrobial soap is superior to alcohol-based hand disinfection dominated until recently. In fact, the latter practice allows much faster hand hygiene during patient care and achieves higher compliance rates.
      • Pittet D.
      Improving adherence to hand hygiene practice: a multidisciplinary approach.
      • Harbarth S.
      • Pittet D.
      • Grady L.
      • et al.
      Interventional study to evaluate the impact of an alcohol-based hand gel in improving hand hygiene compliance.
      Although alcohol-based hand antisepsis has been shown to be superior to hand washing in all important microbiological and technical aspects, the use of alcohol-based hand antisepsis remained limited in US hospitals until the beginning of this century. This is somewhat ironic given that the original observations of Semmelweis were actually related to hand disinfection rather than hand washing with soap and water.
      • Harbarth S.
      Handwashing – the Semmelweis lesson misunderstood?.
      Another misconception is still predominant outside Europe regarding the role of alcohol in skin disinfectants, since alcohol has frequently been overlooked in evidence assessments.
      • Maiwald M.
      • Chan E.S.
      The forgotten role of alcohol: a systematic review and meta-analysis of the clinical efficacy and perceived role of chlorhexidine in skin antisepsis.
      For instance, in a large randomized clinical trial, Darouiche et al. were able to quantify differences in efficacy between two compounds (2% chlorhexidine gluconate and 70% isopropyl alcohol versus an aqueous solution of 10% povidone–iodine) for presurgical skin preparation.
      • Darouiche R.O.
      • Wall Jr., M.J.
      • Itani K.M.
      • et al.
      Chlorhexidine-alcohol versus povidone–iodine for surgical-site antisepsis.
      Results from this study cannot be extended to most European settings as they are based on a comparison with a non-alcoholic iodine compound and centred upon a surgical population with relatively high wound infection rates. As outlined recently by Maiwald and Chan, the perceived efficacy of chlorhexidine is often based on evidence for the efficacy of the chlorhexidine–alcohol combination.
      • Maiwald M.
      • Chan E.S.
      The forgotten role of alcohol: a systematic review and meta-analysis of the clinical efficacy and perceived role of chlorhexidine in skin antisepsis.

      Multicentre interventional research studies

      Several European countries and groups of researchers have helped to increase the evidence base in infection control.
      • Harbarth S.
      • Pittet D.
      Infection prevention research in Europe: recent advances and future priorities.
      Recent examples include multicentre randomized, clinical studies conducted in The Netherlands and France on the prevention of ventilator-associated pneumonia, surgical site infection, and central line-associated bloodstream infection that have gained widespread attention by addressing essential questions of HCAI control.
      • Timsit J.F.
      • Schwebel C.
      • Bouadma L.
      • et al.
      Chlorhexidine-impregnated sponges and less frequent dressing changes for prevention of catheter-related infections in critically ill adults: a randomized controlled trial.
      • de Smet A.M.
      • Kluytmans J.A.
      • Cooper B.S.
      • et al.
      Decontamination of the digestive tract and oropharynx in ICU patients.
      • Bode L.G.
      • Kluytmans J.A.
      • Wertheim H.F.
      • et al.
      Preventing surgical-site infections in nasal carriers of Staphylococcus aureus.
      Furthermore, research funding has increased during the past decade. The European Commission in particular has shaped the research agenda by allocating more than €200 million since 1999, addressing in particular the growing public health threat of antimicrobial resistance.
      • Harbarth S.
      • Pittet D.
      Infection prevention research in Europe: recent advances and future priorities.
      Funded projects included molecular, clinical, and epidemiological studies organized mostly by large-scale, multidisciplinary consortia that have advanced our knowledge and have underlined the leadership role of Europe in this field.
      • Huttner B.
      • Goossens H.
      • Verheij T.
      • Harbarth S.
      Characteristics and outcomes of public campaigns aimed at improving the use of antibiotics in outpatients in high-income countries.
      • Malhotra-Kumar S.
      • Van Heirstraeten L.
      • Lee A.
      • et al.
      Evaluation of molecular assays for rapid detection of methicillin-resistant Staphylococcus aureus.
      • Lee A.
      • Chalfine A.
      • Daikos G.L.
      • et al.
      Hand hygiene practices and adherence determinants in surgical wards across Europe and Israel: a multicenter observational study.
      As mentioned above, the complex, multifaceted nature of HCAI makes the planning and realization of randomized trials difficult, if not unrealistic, in many instances.
      • Harbarth S.
      • Pittet D.
      Infection prevention research in Europe: recent advances and future priorities.
      Therefore, interrupted time-series analyses are a suitable alternative for quasi-experimental research in infection control.
      • Ansari F.
      • Gray K.
      • Nathwani D.
      • et al.
      Outcomes of an intervention to improve hospital antibiotic prescribing: interrupted time series with segmented regression analysis.
      • Harbarth S.
      • Samore M.H.
      Interventions to control MRSA: high time for time-series analysis?.
      These studies should follow rigorous methodological standards, as outlined in an authoritative guideline issued by European experts, called the ‘ORION statement’.
      • Stone S.P.
      • Cooper B.S.
      • Kibbler C.C.
      • et al.
      The ORION statement: guidelines for transparent reporting of outbreak reports and intervention studies of nosocomial infection.
      Of note, the uptake and inclusion of these innovative, but rather complex statistical methods have been quicker and more thorough in European compared with North American research publications.
      • Vernaz N.
      • Sax H.
      • Pittet D.
      • Bonnabry P.
      • Schrenzel J.
      • Harbarth S.
      Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile.
      • Aldeyab M.A.
      • Harbarth S.
      • Vernaz N.
      • et al.
      Quasiexperimental study of the effects of antibiotic use, gastric acid-suppressive agents, and infection control practices on the incidence of Clostridium difficile-associated diarrhea in hospitalized patients.
      • Kaier K.
      • Meyer E.
      • Dettenkofer M.
      • Frank U.
      Epidemiology meets econometrics: using time-series analysis to observe the impact of bed occupancy rates on the spread of multidrug-resistant bacteria.
      • Parienti J.J.
      • Cattoir V.
      • Thibon P.
      • et al.
      Hospital-wide modification of fluoroquinolone policy and meticillin-resistant Staphylococcus aureus rates: a 10-year interrupted time-series analysis.
      Figure 4 shows an example of a recent publication applying interrupted time-series methodology to an interventional cohort study on MRSA control.
      • Lawes T.
      • Edwards B.
      • Lopez-Lozano J.M.
      • Gould I.
      Trends in Staphylococcus aureus bacteraemia and impacts of infection control practices including universal MRSA admission screening in a hospital in Scotland, 2006–2010: retrospective cohort study and time-series intervention analysis.
      Figure thumbnail gr4
      Figure 4Observed trends (red lines) and multivariate transfer model predictions (sum of lagged explanatory variables; black lines) for prevalence density, hospital-associated (HA) incidence density, 30-day mortality in meticillin-resistant Staphylococcus aureus (MRSA) bacteraemia and percentage Staphylococcus aureus bacteraemia (SAB) involving MRSA, Aberdeen Royal Infirmary, Scotland, 2006–2010. AOBDs, acute occupied bed-days. Grey lines, 95% lower and upper confidence limits.
      • Lawes T.
      • Edwards B.
      • Lopez-Lozano J.M.
      • Gould I.
      Trends in Staphylococcus aureus bacteraemia and impacts of infection control practices including universal MRSA admission screening in a hospital in Scotland, 2006–2010: retrospective cohort study and time-series intervention analysis.

      Environmental control

      Traditional, environment-based hospital hygiene has long been considered a weak science, usually arising from the creation of a global hypothesis, which is poetically elaborated upon by its creator without any appeal to patient-orientated facts that would be capable of confirming or refuting it.
      • Harbarth S.
      Epidemiologic methods for the prevention of nosocomial infections.
      • Exner M.
      • Hartemann P.
      • Kistemann T.
      Hygiene and health – the need for a holistic approach.
      There are many examples of environment-focused studies in hospital hygiene that reveal the missed opportunity of introducing some controlled, patient-orientated outcome into the study design.
      • Exner M.
      • Kramer A.
      • Lajoie L.
      • Gebel J.
      • Engelhart S.
      • Hartemann P.
      Prevention and control of health care-associated waterborne infections in health care facilities.
      For instance, a remarkably well-performed longitudinal study about the control of Legionella pneumophila in a hospital water system could have gained clinical importance and generalizability if surveillance data regarding the rate of hospital-acquired legionellosis had been added.
      • Harbarth S.
      • Pittet D.
      • Romand J.
      Fatal concomitant nosocomial legionnaires' disease and cytomegalovirus pneumonitis after cardiac transplantation.
      • Rohr U.
      • Senger M.
      • Selenka F.
      • Turley R.
      • Wilhelm M.
      Four years of experience with silver-copper ionization for control of legionella in a German university hospital hot water plumbing system.
      • Dyck A.
      • Exner M.
      • Kramer A.
      Experimental based experiences with the introduction of a water safety plan for a multi-located university clinic and its efficacy according to WHO recommendations.
      Despite these limitations, the role of the environment as potential reservoir of MDROs has recently gained new momentum.
      • Carling P.C.
      • Parry M.F.
      • Bruno-Murtha L.A.
      • Dick B.
      Improving environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      Several studies from Europe have highlighted the importance of thorough cleaning practices to avoid transmission of MDROs that are capable of surviving in the environment for extended periods.
      • Zanetti G.
      • Blanc D.S.
      • Federli I.
      • et al.
      Importation of Acinetobacter baumannii into a burn unit: a recurrent outbreak of infection associated with widespread environmental contamination.
      • Debast S.B.
      • Vaessen N.
      • Choudry A.
      • Wiegers-Ligtvoet E.A.
      • van den Berg R.J.
      • Kuijper E.J.
      Successful combat of an outbreak due to Clostridium difficile PCR ribotype 027 and recognition of specific risk factors.
      • Longtin Y.
      • Troillet N.
      • Touveneau S.
      • et al.
      Pseudomonas aeruginosa outbreak in a pediatric intensive care unit linked to a humanitarian organization residential center.
      • Wilson A.P.
      • Smyth D.
      • Moore G.
      • et al.
      The impact of enhanced cleaning within the intensive care unit on contamination of the near-patient environment with hospital pathogens: a randomized crossover study in critical care units in two hospitals.
      With respect to hospital cleaning, a broad consensus exists now among European experts that high standards are essential.
      • Dettenkofer M.
      • Ammon A.
      • Astagneau P.
      • et al.
      Infection control – a European research perspective for the next decade.
      This message has also been well received in the USA, where several descriptive and interventional studies addressed the challenge to decrease environmental contamination with MDROs and Clostridium difficile.
      • 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.
      • La Forgia C.
      • Franke J.
      • Hacek D.M.
      • Thomson Jr., R.B.
      • Robicsek A.
      • Peterson L.R.
      Management of a multidrug-resistant Acinetobacter baumannii outbreak in an intensive care unit using novel environmental disinfection: a 38-month report.
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      • Passaretti C.L.
      • Otter J.A.
      • Reich N.G.
      • et al.
      An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms.
      Nevertheless, the impact of environmental contamination on HCAI rates and the cost-effectiveness of surface disinfection as opposed to detergent-based cleaning remains a scientifically unresolved issue, despite a growing body of literature.
      • Dettenkofer M.
      • Ammon A.
      • Astagneau P.
      • et al.
      Infection control – a European research perspective for the next decade.

      Conclusions

      Although prospective, randomized trials are one important method of answering narrow healthcare epidemiology questions, they cannot capture the nuanced, real-world impact of diverse and divergent cultural and practical approaches to infection prevention across international boundaries.
      The Research Committee of the Society of Healthcare Epidemiology of America
      Enhancing patient safety by reducing healthcare-associated infections: the role of discovery and dissemination.
      Cross-country comparison of epidemiological data and infection control practices, a technique that is frequently used in the social sciences, allows an ecological approach that can complement interventional infection control studies based on individual patient-level data.

      Acknowledgements

      This paper is dedicated to the memory of Prof. K. Mühlemann (Berne), who passed away on 1 November 2012. I thank all members of the Infection Control Programme at the University of Geneva Hospitals who have been involved in institutional research projects related to hospital epidemiology and infection control, and Dr A. Huttner for editorial assistance. I am also grateful to Prof. D. Pittet (Geneva, Switzerland), Prof. D. Goldmann (Boston, MT, USA), Prof. Y. Carmeli (Tel Aviv, Israel) and Prof. M. Samore (Salt Lake City, UT, USA) for outstanding mentorship in modern infection control and hospital epidemiology.

      Conflict of interest statement

      S.H. has received consultant and speaker honoraria from bioMérieux (Marcy l'Etoile, France), Da Volterra (Paris, France), and Destiny Pharma (Brighton, UK).

      Funding sources

      S.H. has received research funds from Pfizer (Europe), B. Braun (Germany), the Centre de Recherche Clinique at the Geneva University Hospitals and the European Commission (CHAMP, MOSAR, SATURN, AIDA, R-Gnosis, Rapp-ID and COMBACTE network contracts).

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