Proceedings of The Lancet Conference on Healthcare-Associated Infections

Proceedings of The Lancet Conference on Healthcare-Associated Infections London, UK, 11 12 December 2008 Guest Editor: Professor Kevin G. Kerr

The Official Journal of the Hospital Infection Society Editor S. J. Dancer (Glasgow) Assistant Editors S. P. Barrett (London) J. Bates (Worthing) A. Berrington (Sunderland) J. Child (Worthing) R. Cooke (Liverpool) A. Guyot (Guildford) P. N. Hoffman (London) H. Humphreys (Dublin) T. Inkster (Glasgow) K. Jacobson (Bristol) P. Jumaa (Birmingham) K. G. Kerr (Harrowgate) G. McDonnell (Basingstoke) A. J. Mifsud (London) S. W. B. Newsom (Cambridge) B. Oppenheim (Birmingham) S. Schelenz (Norwich) P. Shears (Wirral) R. C. Spencer (Bristol) J. Stephenson (Surrey) J. Stockley (Worcester) E. L. Teare (Chelmsford) A. M. Walker (Pentraeth) A. P. R. Wilson (London) Reviews I. M. Gould (Aberdeen) Editorial Coordinator N. Atherton Editorial Board P. Astagneau (France) T. S. J. Elliott (Birmingham) A. P. Fraise (Birmingham) C. M. Fry (London) G. Gopal Rao (London) K. Gould (Newcastle) J.-J. Haxhe (Belgium) A. Holmes (London) P. P. Mortimer (London) R. N. Olmsted (USA) J. Philpott-Howard (London) G. L. Ridgway (London) M. Rotter (Austria) E. T. M. Smyth (Belfast) Editorial Advisers G. Ayliffe (UK) F. Daschner (Germany) G. L. French (London) O. B. Jepsen (Denmark) H. Kobayashi (Japan) S. Mehtar (South Africa) J. W. Pearman (Australia) G. Reybrouck (Belgium) H.-G. Sonntag (Germany) A. Voss (Netherlands) Hospital Infection Society Office 162 Kings Cross Road, London WC1X 9DH Tel: 020 7713 0273 Chief Executive Dr T. R. Logan President Dr G. L. Ridgway 162 King s Cross Road, London WC1X 9DH Chairman Dr A. P. Fraise Department of Clinical Microbiology, University Hospital Birmingham NHS Foundation Trust, Queen Elizabeth Medical Centre, Edgbaston, Birmingham B15 2TJ Secretary Ms C. Fry Department of Health, Wellington House, 133 155 Waterloo Road, London SE1 8UG Scientific Secretary Dr T. C. Boswell Department of Microbiology, Queens Campus, Nottingham University Hospitals NHS Trust, Derby Road, Nottingham NG7 2UH Treasurer Dr W. A. Telfer Brunton Department of Clinical Microbiology, Royal Cornwall Hospitals NHS Trust, Penventinnie Lane, Treliske, Truro TR1 3LQ Correspondence G. D. Corcoran (Cork)

VOLUME 73 ISSUE 4 DECEMBER 2009 The Hospital Infection Society The authors, editors, owners and publishers do not accept any respon sibility for any loss or damage arising from actions or decisions arising from information contained in this publication; ultimate responsibility for the treatment of patients lies with the medical practitioner. The opinions expressed are those of the authors and the inclusion in this publication of material relating to a particular product, method or technique does not amount to an endorsement of its value or quality, or of the claims made by its manufacturers. Abstracted/Indexed by: Current Contents, ASCA, Science Citation Index, Infomed, Index Medicus, Medline, EMBASE/Excerpta Medica, Abstracts of Hygiene, Communicable Disease and Tropical Diseases Bulletin and Cumulative Index to Nursing and Allied Health Literature. Contents Introduction Healthcare-associated infection: moving behind headlines to clinical solutions D. Pittet 293 Reviews Historical and changing epidemiology of healthcare-associated infections A. Pearson 296 Role of hand hygiene in healthcare-associated infection prevention B. Allegranzi and D. Pittet 305 Preventing surgical site infection. Where now? H. Humphreys 316 Intravascular catheter infections J. Edgeworth 323 Noroviruses in healthcare settings: a challenging problem M. Koopmans 331 Pseudomonas aeruginosa : a formidable and ever-present adversary K.G. Kerr and A.M. Snelling 338 Extended-spectrum -lactamase-producing organisms M.E. Falagas and D.E. Karageorgopoulos 345 Acinetobacter: an old friend, but a new enemy K.J. Towner 355 Community-associated meticillin-resistant Staphylococcus aureus as a cause of hospital-acquired infections R.L. Skov and K.S. Jensen 364 Screening and isolation for infection control E. Tacconelli 371 The role of environmental cleaning in the control of hospital-acquired infection S.J. Dancer 378 Controversies in infection: infection control or antibiotic stewardship to control healthcare-acquired infection? I.M. Gould 386 Where does infection control fit into a hospital management structure? E.T. Brannigan, E. Murray and A. Holmes 392

Hand hygiene and infection in hospitals: what do the public know; what should the public know? M. Fletcher 397 What are the drivers of the UK media coverage of meticillin-resistant Staphylococcus aureus, the inter-relationships and relative influences? T. Boyce, E. Murray and A. Holmes 400 Are national targets the right way to improve infection control practice? M. Millar 408 Responsibility for managing healthcare-associated infections: where does the buck stop? B.I. Duerden 414 Letter to the Editor Review of Lancet conference on healthcare-associated infections M. Meda 418

Journal of Hospital Infection (2009) 73, 293e295 Available online at www.sciencedirect.com www.elsevierhealth.com/journals/jhin INTRODUCTION Healthcare-associated infection: moving behind headlines to clinical solutions D. Pittet* Infection Control Programme, University of Geneva Hospitals and Faculty of Medicine, 4 Rue Gabrielle- Perret Gentil, 1211 Geneva 14, Switzerland Available online 12 October 2009 Introduction Healthcare-associated infection (HCAI) is universal and complicates patient care both in developed and developing countries. Worldwide, it is estimated that as many as 1.4 million patients acquire infections each day in hospitals alone. 1 Recognising that HCAI prevention is of paramount importance on the current patient safety agenda, The Lancet organised an international conference on HCAI in London in December 2008. What did we learn? Our old friendsdmeticillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), Pseudomonas aeruginosa, Acinetobacter spp., and Clostridium difficiled continue to challenge healthcare settings worldwide. An MRSA pandemic is ongoing and strains are capable of acquiring new virulence factors in addition to multiple resistance. Rapid diagnosis seems useful, but only in conjunction with preventive actions. The screening of target populations deserves further investigation, whereas universal screening appears to be neither effective nor cost-effective. The role of antibiotic * Tel.: þ41 22 372 9828; fax: þ41 22 372 3987. E-mail address: didier.pittet@hcuge.ch pressure on the MRSA reservoir deserves controlled interventions. Importantly, MRSA control is feasible and many examples are available at hospital, regional, or even national levels. VRE spread continues to represent a paradox on both sides of the Atlantic Ocean. VRE is a coloniser of the gut like Gram-negatives, of theskinlikemrsa,andoftheenvironmentlike C. difficile. Thus,VREcontrolmandatesacomplete, multimodal infection prevention strategy, but is clearly feasible. P. aeruginosa remains a key pathogen in hospitals and causes multiple infections. However, the jury is still out on the role of tap-to-patient and patient-to-tap crosstransmission as the reservoir/source. Should P. aeruginosa be considered now as an occupational hazard? Acinetobacter spp. are acquiring pan-resistance to antimicrobials and causing outbreaks, particularly among specific patient populations. In particular, their capacity for long-term survival in the environment complicates control. Should we propose a zero tolerance for P. aeruginosa and Acinetobacter spp.? Extended-spectrum b-lactamase-producing enterobacteriaceae (ESBLs) are now becoming universal with multiple, complex resistance mechanisms that differ worldwide, and studies are needed to better delineate their epidemiology and control. The emergence of a new C. difficile strain over the past years has highlighted major failures in patient safety. Large 0195-6701/$ - see front matter ª 2009 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2009.08.004

294 D. Pittet differences in the disease epidemiology and control are observed among hospitals and countries, but control is feasibledeven at country level. Our old friends are going public: community pathogens are now entering the hospital. Examples include ESBLs and community-acquired MRSA. Norovirus outbreaks originating in the community are affecting institutionalised patient populations, sometimes with devastating consequences. And finally, C. difficile is now responsible for severe community infections among young adults and non-immunocompromised populations in contrast to its more traditional role previously restricted to healthcare settings. Are there clinical solutions? Targeted HCAI prevention is clearly effective. Prevent intravascular line infection? e Yes, we can! How? By using multimodal intervention strategies, sometimes also called bundles. Prevent surgical site infection? e Yes, we possibly can. Again, by decreasing several risk factors, in particular, by the optimal and timely use of perioperative antibiotic prophylaxis. Preventing ventilator-associated pneumonia remains difficult and complex, but is certainly possible using multimodal interventions whose components still need to be defined. In particular, there is a pressing need to revisit the content of the currently proposed bundle strategies. The critical role of setting targets for practice improvement needs to be reviewed, especially at national level. First, healthcare systems should decide what and how to measure. Other questions that follow are: what are the best interventions to implement? What are the targets for improvement? Targets should be set locally considering feasibility and cost-effectiveness. Risk taking is an integral part of healthcare, similar to leadership. In the UK, mandatory surveillance, public reporting, and the setting of performance targets have clearly provided effective leverage. Towards integrated solutions Hand hygiene remains the key measure for HCAI prevention. As illustrated by the successful implementation of the Clean Care is Safer Care multimodal strategy proposed by the World Health Organization First Global Patient Safety Challenge and launched in 2005, promotion is feasible and effective worldwide (http://www.who.int/ gpsc/en). 2 Although environmental control must improve in most healthcare settings with special emphasis on hand-touch sites, it is not the sole responsibility of the infection control team. Cleanliness is everyone s business, from housekeeping to executive staff and board members. There is a clear link between antimicrobial use and resistance at all levels; ward, hospital, regional, country, and even continental. As shown recently through successful nationwide campaigns, the impact of antibiotic control is easier to demonstrate in the community. Infection control teams in hospitals have traditionally worked as fire-fighters and now need to move on to more prevention-oriented stewardship. When wellorganised and effective, antimicrobial stewardship is largely cost-effective. Infection control must be integrated into the hospital management structure at all levels, including the decision-making process. It should use a system-based approach to ensure sustainability, be viewed as a corporate priority, and be based on corporate accountability and institutional leadership. Performance management tools related to infection control metrics are available and HCAI rates can be used as a proxy indicator for differences in system management. The best healthcare model needs to deliver effective, reliable and resilient infection prevention. Should we go public? HCAI is a topic of high public and media interest. However, this increased openness and transparency could also result in a rising concern about the infection risk. As a consequence of the public right to know, public reporting and performance benchmarking is increasingly well-established in several countries. But does it make a difference to the HCAI risk in hospitals and other healthcare settings? Martin Fletcher reviews the evidence on publication reporting and proposes actions for boards and senior leaders to improve the institutional safety culture. 3 He suggests hand hygiene promotion as an exemplar model for increasing patient safety at institutional, regional, or even national level, and the necessity to allow patients to participate in this continuous and complex challenge. It follows, therefore, that communication at all levels must be optimised in the field of infection prevention; it must consider the public right to know, allow patients and families to participate, and work in synergy with the media in multidisciplinary forums that include patients, healthcare workers, scientists, journalists and politicians.

Healthcare-associated infection 295 Infection control is moving behind the headlines to guarantee safer healthcare by applying effective clinical solutions and by conducting research where needed. Infection control is no longer optional. For the sake of every patient in our care, the healthcare community across the globe must make every effort to ensure that it is fully integrated into each institution s management structure. References 1. Lynch P, Pittet D, Borg MA, Mehtar S. Infection control in countries with limited resources. J Hosp Infect 2007; 65(Suppl. 2):148e150. 2. Pittet D, Donaldson L. Clean Care is Safer Care: a worldwide priority. Lancet 2006;366:1246e1247. 3. Fletcher M. Hand hygiene and infection in hospitals: what do the public know; what should the public know? J Hosp Infect 2009;73: 397e399.

Journal of Hospital Infection (2009) 73, 296e304 Available online at www.sciencedirect.com www.elsevierhealth.com/journals/jhin REVIEW Historical and changing epidemiology of healthcare-associated infections A. Pearson a,b, * a Department of HCAI & AMR, Centre for Infections, London, UK b Department of Advanced Computational Biology, University of Maryland, College Park, Maryland, USA Available online 3 November 2009 KEYWORDS Clostridium difficile; Healthcare-associated infection; Medical history; MRSA; Surveillance Summary This review compares the historical perspectives on healthcare-associated infections (HCAIs) with the current changing epidemiological picture as it relates to these infections. Evidence in support of these changes is given using trends in mortality for Clostridium difficile and meticillin-resistant Staphylococcus aureus bacteraemia in England as examples. The impact of current intervention programmes which target these, and other HCAIs, is also considered and knowledge gaps and options for changes in public health strategy required to achieve further reductions in HCAIs in the National Health Service in England are identified. ª 2009 Published by Elsevier Ltd on behalf of The Hospital Infection Society. Historical perspectives In the fourth century BC, Hippocrates, the father of western medicine, is generally attributed as having introduced the need to use treatments for the benefit of the ill in accordance with my ability and my judgment, but from what is to their harm and injustice I will keep them. This is one of a series of statements that were subsequently referred to as the Hippocratic Oath. The oath was an ancient protocol in medicine at the time of Hippocrates although it may not have been * Corresponding address: Department of HCAI & AMR, Centre for Infections, 61 Colindale Avenue, London NW9 5EQ, UK. E-mail address: dandrewpearson@googlemail.com strictly attributable to him. Subsequently the protocol has been adopted universally by medical schools and accreditation bodies including the General Medical Council in the UK. 1 By the twenty-first century AD the Institute for Health Improvement in its 5 Million Lives campaign had enhanced the definition of medical harm as: Unintended physical injury resulting from or contributed to by medical care, including the absence of indicated medical treatment, that requires additional monitoring, treatment or hospitalisation, or that results in death. Such injury is considered harm whether or not it is considered preventable, whether or not it resulted from a medical error or it occurred within a hospital. 2 0195-6701/$ - see front matter ª 2009 Published by Elsevier Ltd on behalf of The Hospital Infection Society. doi:10.1016/j.jhin.2009.08.016

Historical and changing epidemiology of healthcare-associated infections 297 Through the following centuries the Egyptians and Europeans clearly enunciated their interest in medical oversight and culpable negligence. In Egypt, Moses ben Maimon practised and taught medicine insisting on cleanliness as the physician s best friend: Never forget to wash your hands after having touched a sick person and I dismount from my animal, wash my hands, go forth to my patients. In Europe by the nineteenth century several physicians developed further the realisation of the importance of hand washing. Dr Ignaz Semmelweis, the Hungarian-born physician, generally regarded as the father of infection control practice, was responsible in 1847 for the maternity service of the Allgemeine Krankenhaus teaching hospital in Vienna. There he observed that women delivered by physicians and medical students had a much higher rate of post-delivery mortality (13e18%) than women delivered by midwives or trainee midwives (2%). Earlier, less well-evidenced, statements are attributed to Oliver Wendell Holmes: Let the men who mould opinions here look to it; if there is any interested oversight, any culpable negligence and the facts shall reach the public ear, the pestilence-carrier of the lying-in chamber must look to God for pardon, for man will never forgive him. The work of Florence Nightingale in October 1854 and April 1855 made a meticulous analysis of the mortality data and identified poor sanitation as the underlying cause as well as creating new statistical diagrams that persuaded government to reform health. This development of a modernday analytical approach to patient outcome was the evidence base for her Notes on hospitals. This had a profound impact on the design and management of hospitals as it tackled problems of overcrowding in civil hospitals, poor ventilation and lack of cleanliness and reported deaths from preventable diseases, deaths from wounds and deaths from all other causes. HCAI in the twenty-first century The contribution of deaths from HCAI to the total lives lost per year has been estimated by Amalberti who compared healthcare with ultrasafe activities such as flying with scheduled airlines, the nuclear power industry, road traffic deaths, and with dangerous activities such as bungee jumping and mountain climbing. 2 The risk from healthcare is further exemplified by reference to the published mortality reports for C. difficile and meticillin-resistant Staphylococcus aureus (MRSA). Figures 1 and 2 respectively show the UK trends for increasing numbers of death certificates reporting as a cause of death or mentioning C. difficile (1993e2007) and MRSA (1999e 2007). These trends are subject to ascertainment bias as clinicians may change their threshold for notifying deaths due to HCAI. National surveillance and evidence for the changing epidemiology of C. difficile infection Case surveillance based on laboratory reporting is accepted as the most reliable routinely available information by which to measure changes in incidence. In England there are two surveillance systems for measuring S. aureus (including MRSA) and C. difficile infection: voluntary laboratory reporting (LabBase electronic reporting system) and the Department of Health-initiated mandatory MRSA bacteraemia and C. difficile surveillance programmes. The increase in laboratory-confirmed cases of C. difficile infection (CDI) reported to the voluntary national laboratory reporting system between 1990 and 2007 is shown in Figure 3. These English National Health Service (NHS)-based laboratories receive specimens from both hospital and community patients across the whole NHS. Ascertainment during this time varied from around 45% in 1990 to 70% in 2007. Notwithstanding this increased reporting there was a steady increase from 1990 to 2001, after which there was an accelerating rate of increase recognised in retrospect as related to the emergence of newly recognised hyper-toxin-producing strains of C. difficile. Figure 3 also indicates the timelines for the introduction of mandatory surveillance of laboratory-confirmed cases of CDI, mandatory strain surveillance and mandatory enhanced surveillance to monitor a performance target to reduce CDI. In addition the UK Treasury s Public Service Delivery Agreement, published in 2007, introduced a target for a 30% reduction in the number of cases of CDI reported by English NHS hospitals in 2010e11 compared with an agreed baseline in 2007e8. The impact of this mandatory surveillance programme and the setting of a 30% reduction target is seen in Figure 4. Data from the voluntary surveillance shows ascertainment for patients 65 years as 77e85% of the mandatory scheme for each quarter between April 2007 and March 2008. So mandatory surveillance, public reporting and the setting of a performance target was highly effective at increasing ascertainment. This intervention might

298 A. Pearson 9000 8000 Underlying cause Mentions 7000 6000 No. of deaths 5000 4000 3000 2000 1000 0 1999 2000 2001 2002 2003 2004 2005 2006 2007 Year Figure 1 Number of deaths reported with C. difficile as underlying cause or mentioned 1993e2007. Data from the UK Office of National Statistics. itself be expected to influence physicians behaviour. During 2006 and 2007 the Department of Health (DoH) launched the Saving Lives campaign with a High Impact Intervention care bundle to guide physicians and clinical teams in the prevention of CDI. 3 The overall impact of introducing mandatory surveillance, the Saving Lives campaign and the follow-up of NHS trusts against the 1800 1600 Underlying cause Mentions 1400 1200 No. of deaths 1000 800 600 400 200 0 1993 1995 1997 1999 2001 2003 2005 2007 Figure 2 Number of deaths reported with MRSA as underlying cause or mentioned 1999e2007. Data from the UK Office of National Statistics. Year

Historical and changing epidemiology of healthcare-associated infections 299 C. difficile counts 45 000 40 000 35 000 30 000 25 000 20 000 15 000 10 000 5000 0 1990 1991 1992 1993 1994 1995 1996 1997 1998 Year 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 Figure 3 Voluntary NHS laboratory C. difficile surveillance. Timeline for introduction of mandatory surveillance: 2004, mandatory surveillance introduced; 2005, mandatory strain sampling introduced; 2007, mandatory enhanced surveillance introduced. Source: Health Protection Agency LabBase Voluntary Reports; Department of Health Mandatory Surveillance Reports. performance target by a DoH-based improvement team has had a remarkable effect within the first full year of the programme. Figure 5 compares the pattern of changes in rates of CDI per 1000 bed-days. Marked variation across the English NHS underlines both the variability and opportunity for further health gain that exists across the NHS. The enhanced surveillance programme has also begun to provide an insight as to the incidence of CDI in patients aged <65 years as well as in the general population diagnosed with CDI in non-acute care settings. Measurement and the interpretation of enhanced surveillance data from the mandatory scheme is complex but initial analysis indicates that an average of 29% of CDI cases would fit a definition of community-acquired infection based on three categories of specimen: on-presentation cases, cases developing less than 2 days after admission, and non-acute specimens. Aggregate analysis may hide important local variation. This is the case with CDI in the community. The proportion of community CDI cases in local NHS trusts varies markedly from 0 to >55% in a small number of localities. These findings are newly recognised and under further investigation by both epidemiologists and local microbiologists. Early indications are that, as in the past, a proportion of CDI cases do not have either exposure to antibiotics or healthcare as risk factors for their infection. National surveillance and evidence for the reduction in MRSA bacteraemia The laboratory-based voluntary system showed a steep rise in the reported number of MRSA bacteraemia cases between 1990 and 2001 (Figure 6). In 2001, the Chief Medical Officer noted that the prevalence of methicillin-resistant S. aureus has increased markedly in the last decade, primarily associated with hospital acquired infection. 4 Mandatory reporting of MRSA and meticillin-susceptible S. aureus (MSSA) bacteraemia was introduced for all NHS acute trusts in England in April 2001. Enhanced mandatory surveillance was initiated in 2005 which allows cases to be entered in real time and collects more detailed information regarding the incidence and risks of infection. The voluntary reporting system continues to operate alongside the mandatory surveillance scheme. Voluntary surveillance will underestimate the true number of MRSA bacteraemia cases (data not shown). Ascertainment is affected by the number of NHS trusts contributing voluntary data and the completeness of these data, both of which are likely to have varied over time. In total, 30 946 reports of MRSA bacteraemia were made via LabBase between 2002 and 2008. The introduction of mandatory reporting to the web increased this number to 44 344. Mandatory reporting had the greatest impact in the first year when reporting increased by 49% from 4879 to 7274 cases.

300 A. Pearson 18 000 16 000 14 000 12 000 10 000 8000 6000 C. difficile counts 4000 2000 0 Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun 2000 2001 2002 2003 2004 2005 2006 2007 2008 Quarter Figure 4 Comparison of Mandatory and Voluntary NHS laboratory C. difficile surveillance. Solid black line: mandatory 65 years; solid grey line: voluntary 65 years; dashed line: mandatory 2e64 years; dotted line: voluntary 2e64 years. Source: Health Protection Agency LabBase Voluntary Surveillance Reports.

Historical and changing epidemiology of healthcare-associated infections 301 3.50 3.00 2.50 2.00 1.50 C. difficile rate per 1000 bed-days 1.00 0.50 0 2004-2007 2004-2007 2004-2007 2004-2007 2004-2007 2004-2007 2004-2007 2004-2007 2004-2007 East of England East Midlands London North East North West South East South West West Midlands Yorkshire & Humber HPA Region Figure 5 Regional C. difficile rate per 1000 bed-days. HPA, Health Protection Agency. Source: Department of Health Mandatory MRSA bacteraemia surveillance.

302 A. Pearson 16 000 14 000 S. aureus bacteraemia counts 12 000 10 000 8000 6000 4000 MRSA MSSA No susceptibility 2000 0 1990 1991 1992 1993 1994 1995 1996 1997 1998 Year 1999 2000 2001 2002 2003 2004 2005 2006 Figure 6 Staphylococcus aureus bacteraemia voluntary laboratory reporting 1990e2006: meticillin sensitivity reported by English NHS acute trusts. Comparison of the reported numbers to 2008 showed that mandatory reporting has increased ascertainment by between approximately 900 and 2300 cases per year to 39%. The impact of introducing mandatory surveillance, the Saving Lives campaign and the use of improvement teams by the DoH along with a national cleanyourhands campaign has effected the required national reduction of 50% by June 2008 (Figure 7). Again the introduction of mandatory enhanced surveillance of MRSA bacteraemia cases gave a new insight to the epidemiology as it demonstrated that only 65% of cases were acquired during the current hospital admission whereas 34% were reported from patients who were recent admissions from the community or non-acute care facilities. Voluntary submitted risk factor data on 3495/12 483 (28%) cases reported to the mandatory surveillance system between May 2006 and December 2008 indicated key information on the sources of MRSA bacteraemia and highlighted the importance of vascular lines, skin and soft tissue infections as well as other localised infections and urinary tract infections as potentially preventable sources of infection. This is invaluable information on which to base local strategies to further reduce MRSA bacteraemia. So, with the introduction of mandatory surveillance, HCAI has been made a visible and unambiguous indicator of quality and safety of patient care and the Health Protection Agency has provided the NHS with high quality information for the public, patients and clinical teams so that the risks associated with the performance of certain procedures are transparent. Worldwide data on measurement of HCAI is remarkable in its inadequacy. An editorial from leading US senators compared measurement in healthcare and baseball and cited that: Remarkably, a doctor today can get more data on the starting third baseman on his baseball team than on the effectiveness of life-and-death medical procedures. Studies have shown that most health care is not based on clinical studies of what works best. Instead, most care is based on informed opinion, personal observation or tradition. To deliver better health care, we should learn from the successful teams that have adopted baseball s new evidence-based methods. The best way to start improving quality and lowering costs is to study the stats. In the past decade, baseball has experienced a datadriven information revolution. Numbers-crunchers now routinely use statistics to put better teams on the field for less money. Our overpriced, underperforming health care system needs a similar revolution. To deliver better health care, we should learn from the successful teams that have adopted baseball s

Historical and changing epidemiology of healthcare-associated infections 303 2000 1500 MRSA bacteraemias reported 1000 500 0 Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun Jul-Sep Oct-Dec Jan-Mar Apr-Jun 2001 2002 2003 2004 Quarter 2005 2006 2007 2008 Figure 7 Reduction of mandatory MRSA bacteraemia surveillance 2005e2008. Sources: NHS Mandatory and Voluntary MRSA bacteraemia surveillance. new evidence-based methods. The best way to start improving quality and lowering costs is to study the stats. 5 The introduction into the English NHS of a webenabled reporting and user access networked mandatory surveillance system has addressed this deficiency in measurement for a limited number of infections currently targeted by mandatory surveillance and performance management. Knowledge gaps Encouraging though these trends are, current gaps in our knowledge relating to healthcare-associated infection need to be addressed if further reductions in these infections are to be achieved. These include introduction of robust surveillance systems to monitor infections other than those related to MRSA bacteraemia and C. difficile. This should include systematic population-based epidemiological surveillance. Technologies which permit realtime strain characterisation and real-time patient tracking will assist infection control teams in preventing as well as controlling clusters of infection in hospitals at the local level but rapid strain characterisation will be invaluable in recognising changes not only in local but also in regional and national epidemiology. Similarly, real-time electronic prescribing systems will allow enhanced antibiotic audit and better analysis of antibiotic misprescribing which, in turn, will help in efforts to control CDI and antimicrobial resistance. Selective use of improved evidence-based performance management interventions such as reduction targets, never events and zero tolerance will also be beneficial. Finally development and refinement of tools which permit assessment of new interventions to identify how they can be deployed in a cost-effective manner remains a key priority. Conflict of interest statement None declared.

304 A. Pearson Funding sources None. References 1. General Medical Council. Good medical practice: the duties of a doctor registered with the General Medical Council. London: GMC; 2006. 2. Amalberti R. The paradoxes of almost totally safe transportation systems. Saf Sci 2001;37:109e126. 3. Department of Health. Saving Lives: a delivery programme to reduce healthcare associated infection including MRSA. London: DoH; 2006. 4. Department of Health. CMO s update 30: surveillance of healthcare associated infections. London: DoH; 2001. 5. Beane W, Gingrich N, Kerry J. How to take American health care from worst to first. New York Times Online, 24 October 2008.

Journal of Hospital Infection (2009) 73, 305e315 Available online at www.sciencedirect.com www.elsevierhealth.com/journals/jhin REVIEW Role of hand hygiene in healthcare-associated infection prevention B. Allegranzi a, *, D. Pittet a,b a World Alliance for Patient Safety, World Health Organization, Geneva, Switzerland b Infection Control Programme, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland Available online 31 August 2009 KEYWORDS Alcohol-based hand rub; Hand hygiene; Healthcare-associated infection; Intervention; Patient safety; Promotion; World Health Organization Summary Healthcare workers hands are the most common vehicle for the transmission of healthcare-associated pathogens from patient to patient and within the healthcare environment. Hand hygiene is the leading measure for preventing the spread of antimicrobial resistance and reducing healthcare-associated infections (HCAIs), but healthcare worker compliance with optimal practices remains low in most settings. This paper reviews factors influencing hand hygiene compliance, the impact of hand hygiene promotion on healthcare-associated pathogen cross-transmission and infection rates, and challenging issues related to the universal adoption of alcohol-based hand rub as a critical system change for successful promotion. Available evidence highlights the fact that multimodal intervention strategies lead to improved hand hygiene and a reduction in HCAI. However, further research is needed to evaluate the relative efficacy of each strategy component and to identify the most successful interventions, particularly in settings with limited resources. The main objective of the First Global Patient Safety Challenge, launched by the World Health Organization (WHO), is to achieve an improvement in hand hygiene practices worldwide with the ultimate goal of promoting a strong patient safety culture. We also report considerations and solutions resulting from the implementation of the multimodal strategy proposed in the WHO Guidelines on Hand Hygiene in Health Care. ª 2009 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. * Corresponding author. Address: First Global Patient Safety Challenge, World Alliance for Patient Safety, IER/PSP, Room L319, L Building, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland. Tel.: þ41 22 791 2689; fax: þ41 22 791 1388. E-mail address: allegranzib@who.int 0195-6701/$ - see front matter ª 2009 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2009.04.019

306 B. Allegranzi, D. Pittet Introduction Numerous studies document the pivotal role of healthcare workers (HCWs) hands in the propagation of micro-organisms within the healthcare environment and ultimately to patients. 1 As recently described, patient-to-patient transmission of pathogens via HCWs hands involves five sequential steps. 2 Patients skin can be colonised by transient pathogens that are subsequently shed onto surfaces in the immediate patient surroundings, thus leading to environmental contamination. 2 As a consequence, HCWs contaminate their hands by touching the environment or patients skin during routine care activities, sometimes even despite glove use. 2 It has been shown that organisms are capable of surviving on HCWs hands for at least several minutes following contamination. 2 Thus, if hand hygiene practices are suboptimal, microbial colonisation is more easily established and/or direct transmission to patients or a fomite in direct contact with the patient may occur. 2 Based on this evidence and the demonstration of its effectiveness, optimal hand hygiene behaviour is considered the cornerstone of healthcareassociated infection (HCAI) prevention. 2e4 Furthermore, not only is it a key element of standard and isolation precautions, but its importance is emphasised also in the most modern bundle approaches for the prevention of specific site infections such as catheter-related bloodstream infection (CRBSI), catheter-related urinary tract infection (CRUTI), surgical site infection (SSI), and ventilator-associated pneumonia (VAP). 5e9 Together with other specific prevention measures, environmental cleaning is another essential measure to prevent the spread of some pathogens, particularly Clostridium difficile, vancomycin-resistant enterococci (VRE), norovirus, Acinetobacter spp. and meticillinresistant Staphylococcus aureus (MRSA), and should not be neglected. 10e12 Over the past few years, scientific evidence to support the role of hand hygiene in the improvement of patient safety has increased considerably, but some key controversial issues still challenge care practitioners and researchers. This review summarises the key themes on the role of hand hygiene in preventing HCAI. Interpretations and solutions based on the evidence and experience available through the work of the First Global Patient Safety Challenge of the WHO World Alliance for Patient Safety are suggested. Factors influencing hand hygiene compliance It has been known for many years that HCWs encounter difficulties in complying with hand hygiene indications at different levels. 4 Insufficient or very low compliance rates have been reported from both developed and developing countries. 1,4 Reasons which explain suboptimal practices are multiple and may vary according to the setting and the resources available. For example, the lack of appropriate infrastructure and equipment to enable hand hygiene performance, the cultural background, and even religious beliefs can play an important role in hindering good practices. 13e15 The most frequently observed factors determining poor hand hygiene compliance are: (i) belonging to a certain professional category (i.e. doctor, nursing assistant, physiotherapist, technician); (ii) working in specific care areas (i.e. intensive care, surgery, anaesthesiology, emergency medicine); (iii) understaffing and overcrowding; and (iv) wearing gowns and/or gloves. 1 Unfortunately, hand hygiene indications at higher risk of being neglected are the ones that prevent pathogen transmission to the patient (i.e. before patient contact and clean/aseptic procedures). 1 This is also in concordance with the fact that care activities with a higher risk of cross-transmission lead to a higher risk of poor compliance. 1 Individual factors such as social cognitive determinants may provide additional insight into hand hygiene behaviour. 3,16e18 Many factors play a role in eventually determining either a hand hygiene action or lack of compliance: perception and knowledge of the transmission risk and of the impact of HCAI; social pressure; HCWs conviction of their self-efficacy; the evaluation of perceived benefits against the existing barriers; the intention to perform the hand hygiene action. For instance, intention to wash hands did not predict observed handwashing behaviour in one study, whereas it did in another. 19,20 Hence, hand hygiene behaviour appears not to be homogeneous and can be classified into at least two types of practice. 21 Inherent hand hygiene practice, which drives most community and HCW hand hygiene actions, occurs when hands are visibly soiled, sticky or gritty. On the other hand, elective hand hygiene practice represents those opportunities for hand cleansing not encompassed in the inherent category. Among HCWs, this component of hand hygiene behaviour is similar to many common social interactions, such as shaking hands. During healthcare, it would include touching a patient (e.g. taking a pulse or blood pressure) or

Hand hygiene and HCAI prevention 307 having contact with an inanimate object in the patient s surroundings. As they recall a common social behaviour, these contacts do not necessarily trigger an intrinsic need to cleanse hands, although they do involve the risk of cross-transmission. According to behavioural theories, this is the component of hand hygiene most likely to be omitted by busy HCWs and it has been repeatedly confirmed by field observations. Impact of hand hygiene promotion on HCAI Given the complexity of hand hygiene behaviour and the influence of numerous external factors, promotion of good practices is complex and its potential for success depends on the delicate balance between evaluation of benefits and existent barriers. Demonstration of the effectiveness of recommendations and strategies to improve hand hygiene on the ultimate outcome, i.e. the HCAI rate, is crucial in both motivating HCWs behavioural change and securing an investment in this preventive measure by policy-makers and healthcare managers. However, research in this field represents a very challenging activity since methodological and ethical concerns make it difficult to conduct randomised controlled trials with appropriate sample sizes that could establish the relative importance of hand hygiene in the prevention of HCAI. In addition, HCAI surveillance is a very resource- and time-consuming activity requiring rigorous and standardised methods, and therefore is seldom available on a regular and reliable basis. Nevertheless, there is convincing evidence that improved hand hygiene can reduce infection rates. More than 20 hospital-based studies of the impact of hand hygiene on the risk of HCAI have been published between 1977 and 2008 (Table I). 22e45 Of these, some were conducted hospital-wide and report long-term follow-up to demonstrate sustainability. 29,30,38,42 Despite study limitations, almost all reports showed a temporal association between improved hand hygiene practices and reduced infection and cross-transmission rates. Most investigations were conducted in adult or neonatal intensive care units (ICUs) and the large majority introduced the use of alcohol-based hand rubs in association with other promotional components in a multimodal implementation strategy (Table I). Three studies failed to show HCAI reduction following hand hygiene promotion. 24,41,44 In one study, the intervention did not succeed in significantly increasing hand hygiene compliance. 24 In another, the methods and definitions used to detect HCAI were not described and therefore the data reliability cannot be assessed. 44 In a prospective, controlled, cross-over trial, Rupp and colleagues observed no substantial change in device-associated infection rates and infections due to multidrugresistant pathogens, despite a significant and sustained improvement in hand hygiene adherence. 41 Nevertheless, although the study was well designed, it was criticised for lack of screening for cross-transmission, lack of statistical power, and use of an alcohol-based hand rub that failed to meet the EN 1500 standards for antimicrobial efficacy. 46e48 In many countries, the evidence from studies on hand hygiene effectiveness has been convincing enough to motivate governments to invest resources in hand hygiene national and subnational campaigns. 49 However, this evidence mainly reflects findings from interventions implemented in healthcare settings in developed countries. Further research is needed to evaluate the relative efficacy of each key element of multimodal strategies, to assess their implementation feasibility in settings with limited resources, and to gather information on successful solutions allowing adaptation. Among its main objectives, the First Global Patient Safety Challenge, launched by the WHO World Alliance for Patient Safety, intends to make available implementation tools for field use and to assess their validation and adoption in countries at different income levels. 49 Another controversial issue is how significant should be the hand hygiene compliance increase following the intervention in order to be considered satisfactory. No data are available yet to answer this question. Among all the above-mentioned studies, increased compliance rates at follow-up did not exceed 81% (Table I). One study with a follow-up of eight years showed a sustained compliance increase of up to a maximum of 66% and succeeded in parallel to maintain the achieved reduction in HCAI rates of <10%. 29,30 To achieve 100% compliance is not strictly necessary to determine improvement of patient safety at the bedside. On the other hand, the goal of sustained 100% compliance appears unlikely to be achieved because of the complex range of factors influencing HCWs behaviour related to hand hygiene performance. Thus, there is a need for careful consideration before setting a goal of zero tolerance to hand hygiene non-compliance to avoid failure and frustration. Challenging issues related to the adoption of alcohol-based hand rubs The adoption of alcohol-based hand rubs is considered the gold standard for hand hygiene in most

308 B. Allegranzi, D. Pittet Table I Most relevant studies assessing the impact of hand hygiene promotion on HCAI (1977e2008) Year Hospital setting 1977 Adult ICU Promotion of hand washing with a chlorhexidine hand cleanser Intervention Impact on hand hygiene compliance Impact on HCAI Duration of follow-up NA Significant reduction (P < 0.001) in the percentage of patients colonised/infected by Klebsiella spp. Reference 2 years 22 1989 Adult ICU Education on hand washing, hand hygiene observation, performance feedback Compliance increase from 14% to 73% (before patient contact) and from 28% to 81% (after patient contact) Significant reduction (P ¼ 0.02) in HCAI rates (from 33% to 12% and from 33% to 10%, respectively, after two intervention periods 4 years apart) 6 years 23 1990 Adult ICU Hand-washing promotion Compliance increase from 22% to 29.9% No impact on HCAI rates 11 months 24 1992 Adult ICUs Prospective multiple crossover trial on hand hygiene with either chlorhexidine soap or 60% isopropyl alcohol with optional hand washing with plain soap NA Significant reduction (P < 0.02) in HCAI rates using hand washing with chlorhexidine soap 8 months 25 1994 NICU Introduction of hand washing with triclosan 1% (w/v) NA Elimination of MRSA, when combined with multiple other infection control measures. Significant reduction (P < 0.02) in nosocomial bacteraemia (from 2.6% to 1.1%) using triclosan compared with chlorhexidine for hand washing 9 months 26 1995 Newborn nursery Introduction of HCWs hand washing and neonates bathing with triclosan 0.3% (w/v) NA Control of MRSA outbreak 3.5 years 27 2000 MICU/NICU Organisational climate intervention NA Significant (85%) relative reduction (P ¼ 0.02) in VRE rate in the intervention hospital; statistically not significant (44%) relative reduction in control hospital; no significant change in MRSA 8 months 28

Hand hygiene and HCAI prevention 309 2000 Hospital-wide Alcohol-based hand rub introduction, hand hygiene observation, training, performance feedback, posters 2003 Orthopaedic surgical unit Alcohol-based hand rub introduction, posters, feedback on HCAI rates, patient education and involvement 2004 Hospital-wide Alcohol-based hand rub introduction, hand hygiene observation, posters, performance feedback, informal discussions 2004 Adult intermediate care unit Hand hygiene electronic monitoring at exit from patient rooms, direct observation and voice prompts 2004 NICU Alcohol-based hand rub introduction, hand hygiene observation, training, hand-hygiene protocols, posters 2004 NICU Education, written instructions, hand hygiene observation, posters, performance feedback, financial incentives Significant increase in compliance from 48% to 66% Significant reduction (P ¼ 0.04 and P < 0.001) in the annual overall HCAI prevalence (42%) and MRSA cross-transmission rates (87%). Active surveillance cultures and contact precautions implemented during same period. A follow-up study showed continuous increase in hand rub use, stable HCAI rates and cost savings. NA 36% decrease (P value, NA) in HCAI (mainly urinary tract infection and SSI) rates (from 8.2% to 5.3%) No significant increase in compliance before and after patient contact Significant reduction (P ¼ 0.03) in hospital-acquired MRSA cases (from 1.9% to 0.9%) Compliance increase from 19.1% to 27.3% by electronic monitoring Reduction in HCAI rates (not statistically significant, P value, NA) Compliance increase from 40% to 53% (before patient contact) and from 39% to 59% (after patient contact) Reduction (P ¼ 0.14) in HCAI rates (from 11.3 to 6.2 per 1000 patient-days) Compliance increase from 43% to 80% Significant reduction (P ¼ 0.003) in HCAI rates (from 15.1 to 10.7 per 1000 patient-days), in particular for respiratory infections 8 years 29,30 10 months 31 1 year 32 2.5 months 33 6 months 34 2 years 35 (continued on next page)

310 B. Allegranzi, D. Pittet Table I (continued) Year Hospital setting 2005 Hospital-wide Alcohol-based hand rub introduction, hand hygiene observation, training, posters Intervention Impact on hand hygiene compliance Compliance increase from 62% to 81% Impact on HCAI Duration of follow-up Significant reduction (P ¼ 0.01) in hospital-associated rotavirus infections Reference 4 years 36 2005 Adult ICUs Hand-washing observation, training, guideline dissemination, posters, performance feedback Compliance increase from 23.1% to 64.5% Significant reduction (P < 0.001) in HCAI rates (from 47.5 to 27.9 per 1000 patient-days) 21 months 37 2005 Hospital-wide Alcohol-based hand rub introduction, hand hygiene observation, training, posters, promotional gadgets Compliance increase from 21% to 42% Significant reduction (57%, P ¼ 0.01) in MRSA bacteraemia 36 months 38 2007 Neurosurgery Alcohol-based hand rub introduction, training, posters NA Reduction (54%, P ¼ 0.09) in overall incidence of SSI. Significant reduction (100%, P ¼ 0.007) in superficial SSI rates 2 years 39 2007 Neonatal unit Posters, focus groups, hand hygiene observation, HCWs perception assessment, feedback on performance, perception and HCAI rates Compliance increase from 42% to 55% Reduction (P value, NA) in overall HCAI rates (from 11 to 8.2 infections per 1000 patient-days) and 60% decrease (P value NA) in risk of HCAI in very low birth weight neonates (from 15.5 to 8.8 episodes per 1000 patient-days) 27 months 40 2008 ICU Prospective, controlled, cross-over trial in two units with education, posters and alcoholbased hand rub introduction Compliance increase from 38e37% to 68e69% No impact on device-associated infection and infections due to multidrug-resistant pathogens 2 years 41