This article appears in the following Journal of Antimicrobial Chemotherapy issue: The British Society for Antimicrobial Chemotherapy Resistance Surveillance Project 1999/2000-2006/7 [View the issue table of contents]
Articles |
The British Society for Antimicrobial Chemotherapy Resistance Surveillance Project: a successful collaborative model
Tony White Ltd, Newport, Essex, UK
* Tel: +44-77-2531-7702; E-mail: tone_white{at}hotmail.com
| Abstract |
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The British Society for Antimicrobial Chemotherapy (BSAC) Resistance Surveillance Project was initiated in light of the need for UK-wide surveillance of antibacterial resistance in key clinical pathogens. The Project comprises two defined-protocol programmes that cover a range of important pathogens and antibacterials related to community-acquired respiratory tract infection and bloodstream infection, respectively. The Respiratory Programme has reported quantitative susceptibility data for Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis collected from across the UK and Ireland since 1999. The Bacteraemia Programme has reported the susceptibility of a wide range of Gram-positive and -negative organisms since 2001. The sustainability of the Programmes relies on a unique collaborative funding model: sponsorship is provided by a number of pharmaceutical companies in return for the inclusion of their investigational or marketed agents in the study alongside a core panel of established antibacterials. The sponsors have changed over time according to their interest in participating. Results for marketed agents are communicated in a timely manner through the BSAC web site and by presentation and publication, and for investigational agents with the agreement of their sponsors. The Project satisfies the requirement for sustainable defined-protocol high-quality resistance surveillance across the UK and Ireland.
Keywords: respiratory , bacteraemia , longitudinal , national , standardized
| Introduction |
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Effective surveillance is critical to understanding and controlling the spread of resistance stated the UK Standing Medical Advisory Committee (SMAC) Sub-Group on Antimicrobial Resistance in 1998.1 The report from SMAC, entitled The Path of Least Resistance recognized that ...not only does surveillance monitor the existing situation, it allows the effects of interventions to be tested. The Sub-Group recommended that a strategic system for surveillance of antimicrobial resistance, covering the whole of the UK, should be developed as swiftly as possible. It noted that discussions to develop such a system were already taking place between the then Public Health Laboratory Service (PHLS), now incorporated into the Health Protection Agency (HPA), and the British Society for Antimicrobial Chemotherapy (BSAC) and various colleagues in Scotland and Ireland. Importantly, SMAC stated that it was vital that the system being developed was adequately resourced to provide high-quality information.1
A decade later, high-quality data from across the UK and Ireland have been generated and reported annually by the BSAC Respiratory and Bacteraemia Resistance Surveillance Programmes for eight seasons from 1999–2000 to 2006–07 and 6 years from 2001 to 2006, respectively, as part of the BSAC Resistance Surveillance Project.2 The studies have generated quantitative susceptibility data for clinically relevant antibacterial agents and pathogens collected across the UK and Ireland. The studies have been funded through a unique collaboration between the BSAC and the pharmaceutical industry in a way that minimizes the risks associated with a single funding source and which will, it is hoped, allow these and other potential protocols to be sustained.
Quantitative data on antibacterial resistance among key clinical bacterial pathogens are recognized as an important tool in enabling strategies to contain and combat the emergence and spread of resistance and its clinical and societal consequences.1,3,4 Regular assessments of resistance prevalence using a repeatable and reliable methodology allow resistance trends to be assessed and appropriate strategies to be implemented at local, national and international levels. The sustainability of conducting reliable quantitative surveillance programmes over time requires robust protocols that can be adapted as needs arise, but which provide data that (i) can be compared over successive time periods; and (ii) will stand statistical analyses.3,5,6 Sustainability is also dependent on continuous financial support from those who find the data and information of value.3 The surveillance programmes initiated and managed by the BSAC are an example of a successful partnership between a national scientific Society and the pharmaceutical industry. The results are reported and published in a timely manner to the benefit of the Society members, industry partners and the medical/scientific community in general. As such, the BSAC Resistance Surveillance Project represents a unique and pioneering model in conducting sustainable surveillance at the national level.
| Sustainable surveillance: the historical perspective |
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Since the introduction of systemic antibiotics for clinical use in the mid-twentieth century, there have been many and varied studies to assess the susceptibility of the target pathogens to the agents of the day. Such investigations have been conducted at hospital, regional or national levels and have employed methods ranging from comparative disc susceptibility (such as the Stokes method in the UK) to standardized disc susceptibility methods, quantitative MIC determination using broth or agar dilution or the use of automated methodologies. Uniform protocols—though essential to allow comparisons between centres, and over time—were infrequently employed. Rather, comparisons were often compromised by differences in methodology such as inoculum size, medium type and end-point measurements along with sample sizes and collection methodologies.3 As such, surveillance of resistance to antibacterials for nearly the first 50 years of their use was primarily a tool to allow local resistance outbreaks to be monitored or, on a relatively small scale, to allow the activity of new antibacterials to be assessed against emerging and new resistances and compared with established agents. Trends over time, and national prevalences were generally studied, if at all, by reviewing the results from a number of individual studies often with wide-ranging methodologies.
The need to monitor trends in antimicrobial resistance has long been recognized. In the latter half of the 1950s, penicillin resistance in staphylococci had proliferated to such an extent in the UK that an editorial in the BMJ noted that ...the most disquieting feature of present-day hospital practice is the prevalence of antibiotic-resistant staphylococcal infection.7 Bax et al.3 suggest that the hospital pandemic of penicillin-resistant Staphylococcus aureus of the 1950s and 1960s in the UK was probably the starting point of much of the current practice of antibiotic surveillance, but point out that at the time there was a risk of multiple inclusion of successive isolates from infected patients and resultant over-calculation of resistance rates. From the mid-1960s, the emergence of newly recognized plasmid-mediated β-lactamases, such as the TEM-type in Gram-negative bacilli, provided a further impetus for surveillance of emerging resistance.8
In the absence of standardized national longitudinal studies, the assessment of resistance trends over time required considerable effort in obtaining data and in its selection and assessment. For example, in 1993, in order to assess the activity of amoxicillin/clavulanate some 12 years after its introduction into the UK in 1981, and for the 3 years before its launch, Rolinson9 considered over 1500 publications of which 439 were used in the final assessment with, in most countries, no single longitudinal study having been undertaken throughout this period.
Rolinson thus sought to assess any changes in the prevalence of β-lactamase-producing bacterial pathogens and in their susceptibility to amoxicillin/clavulanate by reviewing the data available on each pathogen of interest. With respect to Haemophilus influenzae, for example, studies were only included where they reported data involving the same type of isolates from the same institutions (i.e. like for like) for more than one time period; snap-shot single time point studies were excluded. For serotype b or isolates from invasive infections from 1975 to 1991, there were two UK-based studies, with Broughton et al.10,11 reporting regional (East Anglia) data from 1978, 1980 and 1984. A UK national survey reported every 4–5 years (1977, 1981, 1986 and 1991) and also provided data on non-type b isolates or those from non-invasive infections.12,13 Longitudinal data on β-lactamase production in H. influenzae in the UK were, therefore, regular but infrequent. Data from other countries were, in general, relatively sparse and collected infrequently. There were five studies from the USA, one collecting data annually for 11 years from 1975 to 1985, another annually from 1978 to 1982 with the others reporting infrequently.9 Single studies from Canada, Belgium, France and Australia had data relating only to a few (two to four) years throughout the period and at intervals of 2–5 years.9
To investigate time trends, Rolinson compiled the results of 62 studies from 10 different countries reported from 1978 to 1993 and representing a total of 3066 β-lactamase-producing isolates of H. influenzae. Data for MIC50, MIC90 and MIC100 from each study were compared for each available year. To further establish any change over time, the results for two time periods, 1978–88 and 1989–93, were compared.9 Results of multicentre studies that included both β-lactamase-positive and -negative isolates, from 1983 to 1993, were also used to form a picture of overall susceptibility and were from 11 different studies reporting at different time points, with isolate numbers ranging from 125 to 2458 per study, over seven different countries (Belgium, USA, UK, Ireland, Australia, Canada and Spain) and for which the definition of resistance had been made using different criteria (MIC
1 or
4 mg/L).9 The UK component of this analysis consisted of data from 2458 isolates from 1987 and was assessed using resistance breakpoints of both 1 and 4 mg/L.9,14 A similar overall approach was used to assess the β-lactamase production and susceptibility trends for other key pathogens such as Moraxella catarrhalis, S. aureus, Escherichia coli and Klebsiella species. This extensive analytical approach was necessary as no single longitudinal susceptibility study encompassing the key pathogens was available in 1993, 5 years before the SMAC Report, to provide UK national susceptibility rates over time or to compare data across countries. While the comprehensive analysis of the large amount of data by Rolinson indicated that there had not been any significant increase in resistance to amoxicillin/clavulanate in β-lactamase-producing target bacteria, the existence of standardized defined-protocol longitudinal studies would certainly have made the assessment less onerous. Importantly, such studies might have allowed trends to be assessed more readily and in an ongoing timely manner should resistance have increased over the study period.
The US Centres for Disease Control and Prevention defined surveillance in 1988 as the ongoing and systematic collection, analysis and interpretation of data on disease, the results of which are disseminated to those who need to know and stated that ...such data are used both to determine the need for public health actions and to assess the effects of any intervention program.15 While this definition highlights the essential requirements of surveillance in terms of a planned, ongoing exercise with a defined output and value to end users, Bax et al.3 later highlighted the key problems and pitfalls in implementing such surveillance with regard to antimicrobial resistance. These comprise the need to ensure appropriateness and consistency in choice of drugs and bugs, the selection of host populations to be sampled, the choice of sampling methods and organisms, the susceptibility testing methodology, the handling and reporting of results and, critically, the funding. An additional important consideration is the purpose of surveillance in terms of who it is for, and its geographical scope (global, national and local).3
| Towards standardized national surveillance |
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Standardized national surveillance in the UK was limited at the time of the SMAC report in 1998.1 SMAC reported that some 200 laboratories in England and Wales were submitting susceptibility data for isolates from blood and CSF and that methicillin-resistant S. aureus was being monitored extensively each year, although surveillance of other Gram-positive bacteria was less comprehensive:1 differences in the drugs tested and different methodologies used were some of the criticisms of this approach. Central comprehensive data on multiply drug-resistant enterococci infections were not systematically collected by the PHLS but isolates from England and Wales were submitted on a voluntary basis between 1987 and 1996.1 The susceptibility of Streptococcus pneumoniae was assessed on two occasions with a 5 year interval. All S. pneumoniae isolated at each of the 53 PHLS laboratories in England and Wales during 2 week periods in March 1990 and March 1995 were submitted to the Antibiotic Reference Unit for susceptibility determinations.1,16 This exercise, together with other surveillance undertaken by the PHLS, showed an increase in resistance to penicillin and erythromycin over the 5 years, but not to rifampicin or vancomycin, in isolates from the community or for collated results of isolates from blood or CSF.1,17 Studies to assess emerging resistance in Gram-negative bacteria from blood and CSF were conducted between 1989 and 1997 and reported by the PHLS Communicable Disease Surveillance Centre.1
SMAC observed with respect to these studies that ...at present surveillance of resistance in the UK is limited, and is conducted largely by ad hoc studies by the PHLS, NHS laboratories and universities often sponsored by the pharmaceutical industry.1 It was also noted that the sample sizes for the studies were often small and that the studies were beset by sampling errors. The potential sources of errors were identified as the inclusion of specimens from unresponsive infections, by resistant bacteria being more likely to be sent for testing, specimens more likely to be from tertiary centres and hence more likely to be resistant and the lack of standardized testing.1 A more systematic approach was called for to include the development of a multifaceted national surveillance system comprising alert organism surveillance, reference laboratory monitoring and sentinel laboratory monitoring along with special surveys of defined clinical/bacterial populations.1 The potential considerable cost of defined-protocol studies, particularly over extensive periods of time, along with the notorious lack of standardization and continuing use of the comparative Stokes disc test, was highlighted.1 The BSAC was at the time undertaking a major initiative to supplant such methodology with a better disc test which was then adopted as the PHLS standard operating procedure. Finally, the communication of the results of surveillance to the end users was a key issue that was highlighted as an area for improvement.1
| The way forward |
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A number of potential pitfalls in design and execution of surveillance studies had to be overcome in order to produce reliable comparable data.1,3 High-quality robust surveillance would require protocols encompassing defined clinical populations, clinically or microbiologically relevant organisms or groups of organisms relevant to clinical situations or indications, clinically or microbiologically relevant selection of antibacterials, repeatable standardized quantitative testing methodology and interpretation using clinically relevant and accepted criteria and breakpoints.3 Additionally, sample sizes and the geographical spread and number of centres would need to be sufficient to cover the aims of the study and to allow statistical evaluation. Clinical rather than laboratory denominators would ideally be defined—this still remains an issue particularly with respect to surveillance of isolates from community infections such as from the respiratory and urinary tract. The use of a single central testing laboratory would minimize the potential for methodological differences. Regular communication of results to the target users through presentation and publication would be required so that the data could be acted upon.1,3 Critically, all of this would require extensive and continuous resourcing and funding.1,3
The lack of key longitudinal studies providing uniform surveillance data from which to assess global and national trends, and changes in antibacterial susceptibility of key pathogens, was apparent from Rolinsons review.9 Felmingham et al.18 later noted that at the time (1992), there were few studies in which data were collected in a way that allowed meaningful comparisons to be made between studies, locations or over time. Existing multicentre studies were limited to specific individual countries or geographic regions, mainly Europe or the USA, and it was difficult to establish a picture of how resistance was developing and spreading globally. Furthermore, differences between the use of quantitative versus qualitative data analysis and variations in procedures and interpretative criteria made it difficult to assess the quality of data presented or to compare results between studies, whether within or across countries.18
The problems associated with antibacterial susceptibility surveillance in the early 1990s were not peculiar to the UK alone. In the USA, the American Society for Microbiology (ASM) reported in 1995 from a task force convened to study the prevalence of antibiotic resistance and its associated problems.19 The task force produced a series of recommendations centred around three key elements: (i) education of the physician and the public; (ii) encouragement of more basic research directed to the development of new antimicrobials and vaccines; and (iii) the setting up of a national surveillance system both to confirm and monitor the extent of the problem.19,20 The report made recommendations about the conduct and design of national surveillance, and stated that funding should be a consortium style from all principal parties (government, professional societies and industry).20 Jones later reported in 1996 that no consortium-style funding had been set aside and that the spirit of cooperation and trust needed to deal with this problem appears to be lacking and noted that US Federal Agencies had initiated plans for surveillance without significant input from the other sectors, such as the professions and industry.20 The subsequent experience of the BSAC shows that successful national surveillance can be built around cooperation and collaboration between professional societies, healthcare professionals and industry.
The first multicentre, international, longitudinal study of bacterial susceptibilities of community-acquired respiratory pathogens to a range of agents, tested by standardized methodology in a central laboratory, was the Alexander Project initiated in 1992, pre-dating the recommendations from the ASM and SMAC,18 although results were not reported widely until 1996.21 This study incorporated many of the desirable features of high-quality surveillance in terms of a defined prospective protocol, standardized and controlled methodology and a single testing laboratory. The project studied the susceptibility of the key pathogens implicated in community-acquired respiratory tract infection (RTI) to a wide range of marketed antibacterials.21 The Alexander Project was sustained financially for its duration (1992–2001) by a single source of funding (SmithKline Beecham/GlaxoSmithKline) while the project protocol, methodologies and decisions with respect to interpretation and dissemination of data were managed by a steering committee of independent experts.18,21
During the decade of the Alexander Project, the number of participating centres and countries changed as did the antibacterials tested and the organisms studied, although a core of countries (UK, France, Germany, Italy, Spain, USA) were included for all 10 years.18 The testing methods remained consistent as did the central testing laboratory [GR Micro Ltd, UK (now Quotient Bioresearch Limited, Microbiology, London)], although testing was later strengthened by the use of laboratories at Hershey and Case Western Universities in the USA but with rigorous quality control. Importantly, the use of standardized MIC determinations allowed the reporting of MIC 50, 90 and 100 and the construction of MIC distributions from which changes in emerging resistances and distribution profiles could be visualized, and to which different susceptibility breakpoints could be applied: an important feature as breakpoint criteria can change during the life of a longitudinal project and one that allows comparisons over time with like for like breakpoints.18,21 The bacteria collected and studied were of direct relevance to community-acquired RTI and included H. influenzae, Haemophilus parainfluenzae, M. catarrhalis, S. aureus, S. pneumoniae and Klebsiella pneumoniae at the start of the project, but later reduced to S. pneumoniae, H. influenzae and M. catarrhalis.18,21 The project included up to 27 countries and 27 antibiotics during its 10 year duration.18
The Alexander Project pioneered the design and standards for longitudinal surveillance, along with the associated benefits of a consistent database of antimicrobial susceptibility, enabling changes over time to be assessed. This, along with the retention and storage of the isolates allowed the nature and cause of resistance to be studied further.18 The differentiation of individual and classes of antibacterial agents based on their potency and by the application of PK/PD criteria and associated breakpoints, along with studies of correlations between antibacterial usage and resistance trends over time, and of the evolution of resistance profiles and mechanisms of resistance were additional important scientific benefits.5,18,22
Despite the pioneering aspect and quality of the Alexander Project, it was not a substitute for national longitudinal surveillance studies into the susceptibility of community-acquired RTI pathogens. It highlighted global and national trends, similarities and differences between countries with respect to emerging resistance and mechanisms in S. pneumoniae, H. influenzae and M. catarrhalis and the potential clinical efficacy of the available antibacterials to the emerging resistances. The data were, however, based on only a few centres per country and did not fully reflect local or regional situations in terms of susceptibility prevalences, or provide guidance for local prescribers. While reported frequently at major infectious disease conferences, with some 46 publications and 46 presentations relating to the Project between 1995 and 2004,18 the data were not generally available in an easily usable or timely manner to the practising physician or scientist. The credibility and quality of the Alexander Project was held to be good and was strengthened by the guidance of the independent Steering Committee.18 However, the single source of funding from an individual pharmaceutical company for such a study could raise concerns of design and reporting bias.23 A single funding source also presents a potential risk to long-term sustainability, as management and objectives change within such organizations year on year. Ensuring the budget for each successive year can become an exhausting and uncertain process. Mera et al.5,22 pointed out the shortcomings of the Alexander Project as being related to the ownership and availability of the results, the lack of real-time availability of data, the risk of a single source of funding, the global nature but with few centres in each participating country and, originally, the lack of statistical analysis of the results, which he later addressed. Nevertheless, the Alexander Project displayed important key features that were to be adopted by the BSAC in their objective of providing a sustainable UK-wide surveillance programme. While global in its nature, the Alexander Project set the scene for standardized longitudinal susceptibility surveillance of community-acquired respiratory bacteria and provided a model for other global and national programmes.18
| The BSAC Resistance Surveillance Project |
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An Antibiotic Surveillance Working Group was set up by the BSAC early in 1997, with representatives from the Society, the PHLS and the pharmaceutical industry, and continues today as the Working Party on Resistance Surveillance to manage the BSAC Resistance Surveillance Project.2 The working group defined as a priority the development of a protocol for surveillance of respiratory isolates across the UK and Ireland. In many respects, the protocol borrowed from the Alexander Project in terms of target organisms, collecting methodology and overall philosophy. The number of collecting centres, the test method and interpretative criteria are specific to the UK and Ireland. The BSAC Working Party acts as the core Steering Committee, and recruited in 1999 a dedicated scientific co-ordinator for the Project (Dr Rosy Reynolds).
A key challenge was the structure of the Project in terms of funding. The working group identified a core set of antibacterials for the respiratory programme; namely those in common use and marketed in the UK and Ireland or with scientific relevance to the target organisms, which are tested routinely. Additional antibacterials supplied by sponsoring pharmaceutical companies are tested alongside the core set as research agents. Such agents can be sponsored at any stage in their life, from pre-clinical to marketed and when off-patent or generic. The sponsors have the option of exclusivity to the data on their developmental agents, defined as those without UK or EU marketing authorizations at the time of making the annual sponsorship agreement. For marketed agents, the data can be kept confidential only for a year, after which they have to be released through the BSAC. In practice, many of the sponsors give immediate access to their agents data, and they are put on the web site at the same time as those for the core agents. Data for developmental agents are often included in BSAC presentations with the permission of the sponsors. When a previously developmental agent gains marketing authorization it is usual for all historic data to then be released to the web site, although there is no requirement for this to happen. This approach has not only allowed data on new agents to be generated and published alongside the established core group of agents, but also allowed sponsors to have the option of the benefit of exclusive use of data on their research agents for publication and registration.
The funding model is reliant on a number of sponsors at any one time, and changes according to the agents in which they are interested and as the agents gain regulatory approval and marketing. The approach has, thus far, allowed the continuous funding of both the Respiratory and Bacteraemia programmes. Sponsors and the years in which they participated in the studies are summarized in Tables 1 and 2.
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The BSAC Project monitors resistance to antibacterials across the UK (England, Wales, Scotland and Northern Ireland) and Ireland. Bacterial isolates are collected by a network of laboratories in these countries.2,24 The Project is designed to study the epidemiology of antimicrobial resistance and documents the prevalence of antibacterial resistance (or non-susceptibility), giving MICs and percentage susceptibility for each species/antibiotic (bug/drug) combination tested.2,6 As the study continues, trends in resistance levels over time can be studied by statistical analyses.24 Each programme is designed to monitor the susceptibility of key representative bacterial isolates, collected from clinical centres in the countries of the British Isles.2,6
The Project began initially with the BSAC Respiratory Resistance Surveillance Programme covering community-acquired lower RTI with the collection of the first isolates over the winter of 1999–2000.25–27 At this time, there were four industrial sponsors (Abbott, Aventis/HMR, Bayer and SmithKline Beecham). GR Micro Ltd, London (now Quotient Bioresearch Limited, Microbiology, London), successfully tendered for the role, which continues in 2007/08, as the central testing laboratory. The industrial sponsors have changed over the course of the study with Aventis leaving after the 2000–01 study period, followed by SmithKline Beecham/GlaxoSmithKline (2001–02), Abbott (2002–03) and Bayer (2003–04). Genesoft joined for the 2002/03 season alone, and MSD and Wyeth joined for the 2004–05 study period and remained sponsors up till 2006–07 (Table 1). These changes reflect the interest of the individual companies at any time in generating data from the study.
The Respiratory Programme monitors the susceptibility of lower respiratory tract isolates of S. pneumoniae, H. influenzae and M. catarrhalis collected annually from
20 laboratories across the UK and Ireland.2,25–27 The laboratories submit up to 50 S. pneumoniae and H. influenzae and 25 M. catarrhalis each winter (October–April), excluding samples taken >4 h after hospitalization.24 Some 32 laboratories have contributed since 1999–2000 reflecting changes in the collecting laboratories due to operational or logistical reasons. Antimicrobial MICs are determined and interpreted using BSAC standard methods.2,24–27 Twenty-four antibacterials have been tested to date.
The BSAC Bacteraemia Resistance Surveillance Programme began in January 2001 and covers bloodstream infection.2,28–32 It includes both hospital-acquired infections (nosocomial, healthcare-associated infection) and community-acquired infections. The HPA Antibiotic Resistance Monitoring and Reference Laboratory in London is the central testing laboratory. For the bacteraemia programme,
25 laboratories each submit up to 10 blood isolates from each of 12 main organism groups annually. Since 2001, 30 laboratories have contributed.28–32 As for the Respiratory Programme, MICs are measured and interpreted by standardized BSAC methods.2,23,28–32 The bacteria collected and tested have included Enterobacter spp., E. coli, Klebsiella spp., Proteus spp., Pseudomonas spp., S. aureus, coagulase-negative staphylococci, S. pneumoniae, β-,
- and non-haemolytic streptococci, and Enterococcus spp. along with small numbers of other Gram-negative bacteria (Acinetobacter spp., Citrobacter spp., Serratia spp. and Stenotrophomonas maltophilia).28–32 A total of 34 antibacterials have been tested to date in the bacteraemia programme. The three initial industrial sponsors (MSD, Pfizer/Pharmacia and Wyeth) have remained for the current duration of the study. Subsequently Cubist (2003), Basilea (2003–04), Chiron/Novartis (2005–07), Theravance (2005–07), Johnson and Johnson (2005–07), AstraZeneca (2006–07) and Astellas (2007) have joined in sponsoring the programme (Table 2).
The BSAC Project and its individual programmes continue to be managed by a core Working Party comprising members of BSAC, HPA and the pharmaceutical industry, along with protocol-specific Working Parties including additional representatives from the sponsors and the testing laboratories.
| The value of the BSAC Resistance Surveillance Project |
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As recently as 2004, the Priority Medicines for Europe and the World report from WHO highlighted antibacterial resistance as a priority topic, specifying the need to conduct high-quality surveillance of antibacterial resistance and consumption patterns in hospitals and the community.33 The BSAC Resistance Surveillance Project, in the form of the respiratory and bacteraemia programmes, has provided relevant representative year-on-year high-quality surveillance data from across the UK and Ireland for nearly a decade. The quantitative MIC data have allowed: (i) breakpoints to be applied; (ii) the impact of different breakpoints and methodologies to be assessed; as well as providing (iii) statistical analyses of resistance trends and sampling variabilities.24,34 The data have been presented and published frequently and, importantly, made available to the scientific community via the BSAC web site.2 The site allows the results of the various antibacterial/organism combinations to be viewed in terms of susceptibility (S/I/R), MIC, and MIC distribution. The results from the Project have been reported in 3 peer-reviewed journal publications and 36 presentations, listed in Appendix 2, as well as other publications on data generated from additional studies on the isolates collected in the study.25,28,34 The BSAC holds a collection of 16 550 respiratory isolates and 15 812 bacteraemia isolates that are available for further study on application to the Society.
The BSAC Resistance Surveillance Project fulfils the original call from SMAC for the development of a multifaceted national surveillance system to include surveys of defined clinical/bacterial populations.1 The potential considerable cost of defined-protocol studies, particularly over extended periods of time, along with the notorious lack of standardization highlighted by SMAC, is overcome in the BSAC programmes through joint sponsorship from a number of industry partners, which changes according to the value of the project to them, and through the use of the standardized BSAC susceptibility testing method. The communication of the results to end users, a key issue highlighted by SMAC, is fulfilled through frequent presentation, publication and, importantly, the release of results on the Society web site.2
To an extent this meets the consortium-style funding and the spirit of cooperation and trust that had been identified as a requirement by Jones.20 The funding model for the BSAC programmes does, however, depend on the pharmaceutical industry budgets which, in turn, are dependent on the R&D and marketing funds for new chemical entities in development and pending registration or early launch. More specifically, the project is dependent on UK- and Ireland-based marketing budgets as data generated are generally mainly of specific relevance to these regions. There are ongoing concerns over the future development of new anti-infective agents and the threat of the cessation of research in this field by many major companies. The underlying reasons have been well addressed elsewhere.35–37 A lack of new agents in the development pipelines would jeopardize this model of joint Society–industry funding of national surveillance.
Felmingham et al.18 reported that several criteria had been suggested for determining whether or not a surveillance study provides data useful in the clinical setting. These authors stated that these include: timeliness; accuracy; consistent and standardized methods of collection and analysis, including the use of a central laboratory and internationally accepted standard procedures; the collection of appropriate demographic data; ongoing chronological data collection (year-on-year); quality-control measures; and reporting on major pathogens found in community-acquired or nosocomial infections.18 High-quality surveillance programmes should also be able to identify significant differences, as well as changes and trends in susceptibility to the agents tested.3,18 The reports in this Supplement show the extent to which the BSAC programmes meet these criteria.
While it can be considered that surveillance is vital in the fight against resistance and is the key element to understanding the size of the problem, it alone cannot solve the issue of antibacterial resistance. Nevertheless, a well-planned surveillance study should provide data that will monitor changes in susceptibility and the progress of resistance and thus help in the control of resistance and in the use of the most appropriate antibacterial agents. For the results to be of value, the information gathered must be based on sound studies and be unbiased, and results must be distributed rapidly to those best able to use the data.1,3 The BSAC programmes have to date fulfilled the need for UK/Ireland-based surveillance of resistance trends over time in the important bacterial pathogens associated with community-acquired respiratory infection and hospital- and community-acquired bloodstream infections. The collaborative approach between the Society (BSAC), HPA, Quotient Bioresearch Limited and the pharmaceutical industry has provided high-quality data for nearly a decade. The BSAC project meets the original 1998 SMAC recommendations that a strategic system for surveillance of antimicrobial resistance (incorporating protocol-defined studies), covering the whole of the UK, should be developed and that the system being developed should be adequately resourced to provide high-quality information.1 Furthermore, the information is being generated from sound, unbiased studies and distributed rapidly.
| Funding |
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The BSAC Resistance Surveillance Programmes up to 2006 (bacteraemia) and 2006/07 (respiratory) have received financial support from Abbott, AstraZeneca, Aventis, Basilea, Bayer, Cubist, GeneSoft, GlaxoSmithKline, Johnson & Johnson, Merck Sharp & Dohme, Novartis, Pfizer, Theravance, Wyeth or their predecessors. The BSAC funds the work of the Resistance Surveillance Coordinator and Resistance Surveillance Working Party.
| Transparency declarations |
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This article is part of a Supplement sponsored by the British Society for Antimicrobial Chemotherapy.
A. R. W. is an Independent Consultant, a retired employee and shareholder of GlaxoSmithKline (GSK), and has received financial remuneration for consultancy or presentations from GSK, and Chiron/Novartis. A. R. W. is a core member of the BSAC Surveillance Working Party and serves on BSAC Council.
| Appendix 1 |
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Acknowledgements. We would like to thank the many colleagues who have contributed to the work of the BSAC Resistance Surveillance Project from 1999 to the present.
BSAC Working Parties on Resistance Surveillance—current members (May 2008)
Core: Alasdair MacGowan (Chair; Southmead Hospital, Bristol), Rosy Reynolds (Co-ordinator; Southmead Hospital, Bristol), Derek Brown (HPA, Addenbrookes Hospital, Cambridge), David Felmingham (Quotient Bioresearch Ltd, Microbiology), Deirdre Lewis (HPA SouthWest), David Livermore (HPA), Christopher Thomson (IMS Health) and Anthony White (Tony White Ltd). Central Laboratories: Russell Hope (HPA), Kirsty Maher (Quotient Bioresearch Ltd, Microbiology) and Ian Morrissey (Quotient Bioresearch Ltd, Microbiology). Sponsors: Michael Allen (Novartis), Karen Bush (Johnson & Johnson Pharmaceutical Research & Development), Rita Charters (Astellas Pharma Europe Ltd), Nicholas Deaney (Merck Sharp & Dohme Ltd), Jeremy Dennison (Pfizer Ltd), Mohamed Lockhat (AstraZeneca UK Ltd) and Christopher Longshaw (Wyeth Laboratories).
Central Laboratory for Respiratory Resistance Surveillance Programme—Quotient Bioresearch Limited, Microbiology, London
Alex Colclough, David Felmingham, James Huff, Kirsty Maher, Ian Morrissey, Jemma Shackcloth, Kirsten Stone, Andrea Williams and Laura Williams.
Central Laboratory for Bacteraemia Resistance Surveillance Programme—Health Protection Agency Centre for Infections, London
Antibiotic Resistance Monitoring and Reference Laboratory
Geraldine Brick, Melissa Coleman, Tess Gatward, Caroline Henwood, Russell Hope, Dorothy James, David Livermore, Teresa Parsons, Rachel Pike, Nicola Potz, Rachel Walker, Marina Warner and Neil Woodford.
Respiratory and Systemic Infections Laboratory
Karen Broughton, Chenchal Dhani, Androulla Efstratiou, Michaela Emery, Robert George and Siobhan Martin.
Supply of isolates for repeated testing
Derek Brown (Addenbrookes Hospital, Cambridge) and Jennifer Andrews (City Hospital, Birmingham).
Collecting Laboratories—Respiratory
England: City Hospital, Birmingham; Wolverhampton New Cross Hospital, Birmingham; Walsall Manor Hospital, Birmingham; Southmead Hospital, Bristol; Addenbrookes Hospital, Cambridge; Queen Elizabeth Hospital, Gateshead; St Jamess University Hospital, Leeds; Leeds General Infirmary, Leeds; Royal Infirmary, Leicester; University of Liverpool, Liverpool; Barts and The London, London; University College Hospitals, London; Salford Hope Hospital, Manchester; Royal Victoria Infirmary, Newcastle; Freeman Hospital, Newcastle; Derriford Hospital, Plymouth; Southampton General Hospital, Southampton; and Sunderland Royal Hospital, Sunderland. Wales: University Hospital of Wales, Cardiff; and Wrexham Maelor Hospital, Wrexham. Scotland: Royal Infirmary, Aberdeen; Western General Hospital, Edinburgh; New Royal Infirmary, Edinburgh; Glasgow Royal Infirmary, Glasgow; Southern General Hospital, Glasgow; and Wishaw General Hospital, Wishaw. N. Ireland: Royal Hospitals, Belfast; and Ulster Dundonald Hospital, Belfast. Ireland: Meath, Adelaide & National Childrens Hospital, Dublin; St Vincents Hospital, Dublin; Beaumont Hospital, Dublin; and University College Hospital, Galway.
Collecting Laboratories—Bacteraemia
England: William Harvey Hospital, Ashford; City Hospital, Birmingham; Bristol Royal Infirmary, Bristol; West Suffolk Hospital, Bury St Edmunds; Addenbrookes Hospital, Cambridge; Chelmsford Public Health Laboratory, Chelmsford; Countess of Chester Hospital, Chester; Coventry & Warwickshire Hospital, Coventry; Royal Infirmary, Leicester; St Marys Hospital, London; University College Hospital, London; Wythenshawe Hospital, Manchester; South Cleveland Hospital, Middlesbrough; Freeman Hospital, Newcastle; Norfolk & Norwich Hospital, Norwich; University Hospital, Nottingham; Northern General Hospital, Sheffield; Royal Shrewsbury Hospital, Shrewsbury; Southampton General Hospital, Southampton; Sunderland Royal Hospital, Sunderland; and Treliske Hospital, Truro. Wales: Ysbyty Gwynedd, Bangor; and University Hospital of Wales, Cardiff. Scotland: Ninewells Hospital, Dundee; Glasgow Royal Infirmary, Glasgow; and Victoria Hospital, Kirkcaldy. N. Ireland: Belfast City Hospital, Belfast; and Altnagelvin Area Hospital, Londonderry. Ireland: Cork University Hospital, Cork; and Beaumont Hospital, Dublin.
BSAC Surveillance Website—MRS Web Solutions Ltd
Carol Blackford-Mills, Thushara Pethiyagoda and Robert Reid.
BSAC Headquarters staff
Jacqui Bramma, Christine Burley, Tracey Guise and Philippa McCoy.
BSAC Working Parties on Resistance Surveillance—former members (from 1999)
Core: R. Bax (SmithKline Beecham) J. Edwards (Zeneca) and R. Wise (City Hospital, Birmingham). Central Laboratories: GR Micro/Quotient Bioresearch Ltd—J. Shackcloth and L. Williams. HPA—C. Henwood, N. Potz, R. Walker and A. Williams. Website: Micron Research—I. Harding and V. Reed. Sponsors: S. Barrière (Theravance), J. Booth (Bayer), C. Burley (Bayer), M. Byrne (Chiron), S. Coles (Abbott), T. Cooper (Abbott), K. Crook (GSK), V. Heaton (Bayer), R. Hennings (Chiron), F. Hughes (GSK), R. Junor (Pfizer), D. Lofland (GeneSoft), A. McDougle (GSK), L. Moore-Ramdin (Wyeth), S. Sivakumaran (Aventis), G. Thorne (Cubist), P. Turner (AstraZeneca), J. Van Tam (GSK), B. Ward (MSD), P. Watson (Novartis), J. Willcock (Aventis) and R. Wiltshire (Pfizer).
The BSAC itself funds the work of the Resistance Surveillance Co-ordinator and Resistance Surveillance Working Party. The BSAC Resistance Surveillance Project has received financial support from Abbott, Astellas, AstraZeneca, Aventis, Basilea, Bayer, Cubist, GeneSoft, GlaxoSmithKline, Johnson & Johnson, Merck Sharp & Dohme, Novartis, Pfizer, Theravance, Wyeth or their predecessors, at times between 1999 and 2007. The charts below show their periods of association with the project and the antimicrobial agents they have contributed for testing.
Several papers here have made extensive use of the HPA LabBase database for comparison with BSAC surveillance data. We would like to thank all the laboratories that have contributed data for bacteraemia isolates to LabBase, and Alan Johnson, Mark Lillie, Andrew Pearson and Georgia Duckworth who have co-ordinated this project and made data available from it.
Respiratory Resistance Surveillance Programme—financial support and contributed agents.
Bacteraemia Resistance Surveillance Programme—financial support and contributed agents
| Appendix 2 |
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|
|
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Publications from the BSAC Antimicrobial Resistance Surveillance Project to June 2008. The previous publications listed below are based on sections of the data now presented more fully in the papers of this Supplement.
- Reynolds R, Potz N, Colman M et al. Antimicrobial Susceptibility of the Pathogens of Bacteraemia in the UK and Ireland 2001–2002: the BSAC Bacteraemia Resistance Surveillance Programme. J Antimicrob Chemother 2004; 53: 1018–32.
- Reynolds R, Shackcloth J, Felmingham D et al. Antimicrobial susceptibility of lower respiratory tract pathogens in Great Britain and Ireland 1999–2001 related to demographic and geographical factors: the BSAC Respiratory Resistance Surveillance Programme. J Antimicrob Chemother 2003; 52: 931–43.
- Reynolds R, Shackcloth J, Felmingham D et al. Comparison of BSAC agar dilution and NCCLS broth microdilution MIC methods for in vitro susceptibility testing of Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis: the BSAC Respiratory Resistance Surveillance Programme. J Antimicrob Chemother 2003; 52: 925–30.
- 4. Reynolds R, BSAC Working Parties on Resistance Surveillance. Unsuitability of MIC50, MIC90 for comparison of antibiotic potency. Clin Microbiol Infect 2008; 14 Suppl 7: S606 (abstract P2059).
- 5. Reynolds R, Felmingham D, Williams L et al. BSAC Respiratory Resistance Surveillance Programme Update 2006–07. In: Abstracts of the Federation of Infection Societies (FIS) Scientific Meeting, Cardiff, UK, 2007. Abstract P025, p. 31.
- 6. Reynolds R, Hope R, Livermore DM et al. BSAC Bacteraemia Resistance Surveillance Programme Update 2006. In: Abstracts of the Federation of Infection Societies (FIS) Scientific Meeting, Cardiff, UK, 2007. Abstract P024, p. 30.
- 7. Reynolds R, Lambert P, Burton P et al. Resistance surveillance studies: methods to prevent invalidation by inter-centre variation. In: Abstracts of the 47th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Chicago, IL, 2007. Abstract C2-2039, p. 144. American Society for Microbiology, Washington, DC, USA.
- 8. Reynolds R, Hope R, BSAC Working Party on Bacteraemia Resistance Surveillance. Resistance still rising in Enterobacteriaceae from Blood in the UK and Ireland. In: Abstracts of the 47th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Chicago, IL, 2007. Abstract C2-2036, p. 143. American Society for Microbiology, Washington, DC, USA.
- 9. Reynolds R, Hope R, BSAC Working Party on Bacteraemia Resistance Surveillance. Species differences in antimicrobial resistance among coagulase-negative staphylococci from blood in the UK and Ireland. In: Abstracts of the 47th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Chicago, IL, 2007. Abstract C2-138, p. 99. American Society for Microbiology, Washington, DC, USA.
- 10. Reynolds R, Felmingham D, Hope R et al. Comparison between respiratory and blood isolates of community-acquired Streptococcus pneumoniae from the UK and Ireland: resistance and serotypes. Clin Microbiol Infect 2007; 13 Suppl 1: S179 (abstract P732).
- 11. Reynolds R, Hope R, BSAC Working Party on Bacteraemia Resistance Surveillance. Resistance in Pseudomonas aeruginosa and Acinetobacter spp. from blood in the UK and Ireland, 2001–2005. Clin Microbiol Infect 2007; 13 Suppl 1: S77 (abstract O363).
- 12. Livermore DM, Reynolds R, Hope R et al. BSAC Bacteraemia Resistance Surveillance Programme Update 2005. In: Abstracts of the Federation of Infection Societies (FIS) Conference, Cardiff, UK, 2006. Abstract P086, p. 45.
- 13. Reynolds R, Felmingham D, Williams L et al. BSAC Respiratory Resistance Surveillance Programme Update 2005–06. In: Abstracts of the Federation of Infection Societies (FIS) Conference, Cardiff, UK, 2006. Abstract P085, p. 45.
- 14. Reynolds R, Felmingham D, BSAC Working Parties on Resistance Surveillance. Analysing Resistance Surveillance Data: the Importance of Inter-centre Variation. In: Abstracts of the 46th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), San Francisco, CA, 2006. Abstract C2-1832, p. 138. American Society for Microbiology, Washington, DC, USA.
- 15. Reynolds R, Hope R, BSAC Working Party on Bacteraemia Resistance Surveillance. Trends in resistance of Staphylococcus aureus from blood in the UK and Ireland 2001–2005, and activity of telavancin in 2005. In: Abstracts of the 46th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), San Francisco, CA, 2006. Abstract C2-1143, p. 124. American Society for Microbiology, Washington, DC, USA.
- 16. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. Stable or falling antimicrobial resistance in community-acquired respiratory pathogens in the UK: a six-year study. In: Abstracts of the 46th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), San Francisco, CA, 2006. Abstract C2-422, p. 111. American Society for Microbiology, Washington, DC, USA.
- 17. Reynolds R, Hope R, BSAC Working Party on Bacteraemia Resistance Surveillance. Activity of doripenem in the context of rising antimicrobial resistance in invasive Enterobacteriaceae in the UK and Ireland. In: Abstracts of the 46th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), San Francisco, CA, 2006. Abstract C2-65, p. 93. American Society for Microbiology, Washington, DC, USA.
- 18. Reynolds R, Hope R, BSAC Working Party on Bacteraemia Resistance Surveillance. Trends in resistance of bacteraemia isolates in the UK and Ireland and current activity of ceftobiprole. Clin Microbiol Infect 2006; 12 Suppl 4: (abstract P1386).
- 19. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. Activity of ertapenem and tigecycline against recent isolates from community-acquired lower respiratory infections in the UK and Ireland. Clin Microbiol Infect 2006; 12 Suppl 4: (abstract P1385).
- 20. Reynolds R, Hope R, BSAC Working Party on Bacteraemia Resistance Surveillance. Rising ESBL production and ciprofloxacin resistance in invasive Enterobacteriaceae in the UK and Ireland. In: Abstracts of the 45th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Washington, DC, 2005. Abstract C2-778, p. 117. American Society for Microbiology, Washington, DC, USA.
- 21. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. Reliability of routinely-generated data for surveillance of resistance in Streptococcus pneumoniae and Haemophilus influenzae in the UK and Ireland. In: Abstracts of the 45th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Washington, DC, 2005. Abstract C2-276, p. 103. American Society for Microbiology, Washington, DC, USA.
- 22. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. Fluoroquinolone resistance and its association with other resistances in Streptococcus pneumoniae in the UK and Ireland. In: Abstracts of the 45th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Washington, DC, 2005. Abstract C2-236, p. 92. American Society for Microbiology, Washington, DC, USA.
- 23. Reynolds R, Hope R, BSAC Working Party on Bacteraemia Resistance Surveillance. Antimicrobial susceptibility among invasive Gram-positive bacteria in the UK and Ireland: the BSAC bacteraemia resistance surveillance programme 2003. Clin Microbiol Infect 2005; 11 Suppl 2: 664 (abstract R1999).
- 24. Reynolds R, Hope R, BSAC Working Party on Bacteraemia Resistance Surveillance. Antimicrobial susceptibility among invasive Gram-negative bacteria in the UK and Ireland: the BSAC bacteraemia resistance surveillance programme 2003. Clin Microbiol Infect 2005; 11 Suppl 2: 591 (abstract P1793).
- 25. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. Influence of age on resistance in community-acquired lower respiratory tract isolates of S. pneumoniae from the UK and Ireland. Clin Microbiol Infect 2005; 11 Suppl 2: 470 (abstract P1454).
- 26. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. 5-year trends in resistance among community-acquired lower respiratory tract isolates of S. pneumoniae from the UK and Ireland. Clin Microbiol Infect 2005; 11 Suppl 2: 469 (abstract P1453).
- 27. Reynolds R, Livermore DM, BSAC Working Party on Bacteraemia Resistance Surveillance. Effect of culture conditions on MICs of BAL9141, representing a new class of cephalosporins active against MRSA. In: Abstracts of the 44th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Washington, DC, 2004. Abstract E-2036, p. 181. American Society for Microbiology, Washington, DC, USA.
- 28. Reynolds R, Livermore DM, BSAC Working Party on Bacteraemia Resistance Surveillance. Comparative activity of BAL9141, daptomycin and linezolid vs. S. aureus from bacteremias in the UK and Ireland. In: Abstracts of the 44th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Washington, DC, 2004. Abstract E-2035, p. 180. American Society for Microbiology, Washington, DC, USA.
- 29. Reynolds R, Potz N, BSAC Working Party on Bacteraemia Resistance Surveillance. Comparison of antimicrobial resistance in hospital-acquired and community-acquired bacteraemia. Clin Microbiol Infect 2004; 10 Suppl 3: 329 (abstract P1196).
- 30. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. Trends in β-lactam resistance in community-acquired lower respiratory tract infection in the UK and Ireland. Clin Microbiol Infect 2004; 10 Suppl 3: 309 (abstract P1134).
- 31. Reynolds R, Potz N, BSAC Working Party on Bacteraemia Resistance Surveillance. Suitability of current routinely generated data for surveillance of antimicrobial resistance of Escherichia coli and Pseudomonas aeruginosa in the UK and Ireland. Clin Microbiol Infect 2004; 10 Suppl 3: 298 (abstract P1100).
- 32. Reynolds R, Potz N, BSAC Working Party on Bacteraemia Resistance Surveillance. Activity of tigecycline against 2206 recent bacteremia isolates in the UK and Eire. In: Abstracts of the 43rd Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Chicago, IL, 2003. Abstract E-1532, p. 206. American Society for Microbiology, Washington, DC, USA.
- 33. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. Comparative prevalence of antimicrobial resistance in community-acquired lower respiratory Streptococcus pneumoniae from countries of the UK, and from Eire. In: Abstracts of the 43rd Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Chicago, IL, 2003. Abstract C2-941, p. 131. American Society for Microbiology, Washington, DC, USA.
- 34. Reynolds R, Potz N, BSAC Working Party on Bacteraemia Resistance Surveillance. Prevalence of antimicrobial resistance in bacteremia isolates from teaching and non-teaching hospitals in the UK and Eire. In: Abstracts of the 43rd Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Chicago, IL, 2003. Abstract C2-187, p. 122. American Society for Microbiology, Washington, DC, USA.
- 35. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. Multiple resistance is rare in community-acquired lower respiratory tract infection in the UK and Ireland. Clin Microbiol Infect 2003; 9 Suppl 1: 94 (abstract P483).
- 36. Reynolds R, Felmingham D, Livermore DM et al. Susceptibility to penicillin of invasive compared with respiratory Streptococcus pneumoniae and relationship with age. Clin Microbiol Infect 2003; 9 Suppl 1: 7 (abstract O66).
- 37. Reynolds R, Felmingham D, BSAC Working Party on Respiratory Resistance Surveillance. Susceptibility patterns are unchanged over three years in community-acquired lower respiratory Streptococcus pneumoniae and Haemophilus influenzae in the UK and Ireland. Clin Microbiol Infect 2003; 9 Suppl 1: 7 (abstract 066).
- 38. Reynolds R, Felmingham D. The antimicrobial susceptibility of Streptococcus pneumoniae in community-acquired lower respiratory tract infection varies with patient age. In: Abstracts of the 42nd Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), San Diego, CA, 2002. Abstract C2-1635, p. 111. American Society for Microbiology, Washington, DC, USA.
- 39. Reynolds R, Livermore DM. Resistance among the pathogens of bacteremia in the UK assessed by sentinel surveillance and routine data. In: Abstracts of the 42nd Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), San Diego, CA, 2002. Abstract C2-302, p. 90. American Society for Microbiology, Washington, DC, USA.
- 40. Reynolds R, MacGowan AP, Felmingham D et al. Conversion between NCCLS microdilution and BSAC agar dilution methods for respiratory pathogens. In: Abstracts of the 41st Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Chicago, IL, 2001. Abstract D-173, p. 152. American Society for Microbiology, Washington, DC, USA.
- 41. Reynolds R, MacGowan AP, Felmingham D et al. Antimicrobial susceptibility of community-acquired respiratory pathogens in Ireland compared with England, Wales and Scotland. In: Abstracts of the 41st Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Chicago, IL, 2001. Abstract C2-683, p. 128. American Society for Microbiology, Washington, DC, USA.
- 42. Reynolds R, BSAC Extended Working Party on Respiratory Resistance Surveillance. BSAC Respiratory Resistance Surveillance Programme: first results of the winter 1999–2000 collection. In: Abstracts of the 22nd International Congress of Chemotherapy (ICC), Amsterdam, The Netherlands, 2001. Abstract P27.088, p. S143. Int J Antimicrob Agents; 17 Suppl 1.
- 5. Reynolds R, Felmingham D, Williams L et al. BSAC Respiratory Resistance Surveillance Programme Update 2006–07. In: Abstracts of the Federation of Infection Societies (FIS) Scientific Meeting, Cardiff, UK, 2007. Abstract P025, p. 31.
| Acknowledgements |
|---|
We are grateful to all who have contributed to the success of the BSAC Resistance Surveillance Project, in particular the many laboratories that have collected isolates and all who have played a part in testing them [see page ii10 (Acknowledgements)] along with past and present members of the BSAC Resistance Surveillance Working Party. Additional information on the isolates collected in the Project is available on the BSAC web site (www.bsacsurv.org, or through a link on the BSAC homepage www.bsac.org.uk). See page ii12 (Publications) for a full list of previous publications from the Project, some of which may include parts of the information presented here.
A. R. W. is grateful to Rosy Reynolds and David Livermore for review and comments on the manuscript.
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