Introduction

Healthcare-associated infections (HCAI) are increasingly important as a public health issue, and these infections are of concern to healthcare workers, patients and the public [1–3]. According to the World Health Organisation (WHO), the prevalence of HCAI in developed countries ranges between 3.5 and 12.0 % [2]. In a 2011–2012 survey of over 1000 hospitals in 13 countries, 6.0 % of patients in European hospitals had an HCAI, increasing fourfold to 19.5 % of patients in intensive care units, and one in three patients received an antimicrobial agent on any given day [4]. Whilst HCAIs are multifactorial and include the underlying complexity of the patient’s condition, e.g., cancer, it is acknowledged that many HCAIs are preventable and that significant cost savings could be made by the more rigorous application of established best practice.

In addition to the need to prevent HCAI, there is increasing concern about multidrug-resistant bacteria and the lack of alternatives to currently available agents. It has been suggested that there needs to be more international cooperation to facilitate the development, evaluation and introduction of novel antimicrobial drugs and technologies, as well as infection prevention and control strategies [5, 6]. Amongst the most challenging issues are resistant Gram-negative bacilli, where there is international spread between countries with many challenges in prevention and control because of the multiple resistance mechanisms and the many potential reservoirs [7, 8].

Many efforts are underway locally, nationally and internationally to prevent and control HCAIs and antimicrobial resistance. Earlier diagnosis and the more appropriate use of antimicrobial agents are important, and the European Union (EU) has funded research projects on these topics, such as the European network for mastering hospital antimicrobial resistance (MOSAR) [9]. Also, in many countries, there has been (and still is) particular emphasis on improving compliance with hand hygiene recommendations, a process supported by international experts, most governments and the WHO [10]. However, it is not clear what professionals in the area of HCAI prevention and control believe should be the key priorities. There is a danger that, in the absence of a clear focus and a defined strategy, efforts and time may be wasted in not tackling HCAI appropriately if these important stakeholders are not considered.

Here, we report the priorities for HCAI prevention and control judged by experts in the area, as revealed in an international survey that was carried out in early 2013.

Methods

The survey was organised by the European society of clinical microbiology and infectious diseases (ESCMID) Study Group for Nosocomial Infections (ESGNI). The survey was piloted amongst the members of the ESGNI Co-ordinating Study Group and focussed on seven topics that were felt to be of particular importance, i.e., surveillance, economics/mathematical models, microbial epidemiology and resistance, organisational and behavioural change, healthcare delivery factors, specific HCAI and settings, and decolonisation/disinfection/antiseptics (details available in supplementary material). Antimicrobial stewardship was not included as it is the subject of another ESCMID study group and has been addressed elsewhere.

On 1st February 2013, the survey achieved approval of the ESCMID Scientific Affairs Officer (Murat Akova). Following this, it was transformed into SurveyMonkey® [11] and (after pretesting) put on the ESCMID homepage. An e-mail message was distributed from the ESCMID Executive Office (H.S.) to international experts in infection prevention and control through use of the ESGNI/ESCMID Newsletter, thus targeting about 5000 individuals. Participants were able to complete the survey between 13th February and 28th March 2013. For each question, the participant was asked to give a rating from one (very low importance) to ten (of extraordinary importance) for the seven topics as well as for each component of the topic or subtopic. There was no restriction on the participant giving equal importance to more than one topic or subtopic. The survey was open to all infection prevention and control practitioners in the EU and beyond.

Results

During the survey period, 589 participants from 86 countries (from five continents and 16 subcontinents) completed the survey (response rate: 11.8 %). The highest number of participants, i.e., 462, were from Europe, with Western Europe (151), Southeastern Europe (125) and Southwestern Europe (107) being the most commonly represented. There were 63 participants from Asia, 33 from the Americas, 21 from Africa and 10 from Oceania. Figure 1 illustrates the distribution of respondents in Europe.

Fig. 1
figure 1

Distribution of participants from European countries (with ≥5 participants)

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Physicians accounted for over 60 % of the participants followed by scientists (20 %) and others at 14 %. The highest medical group represented amongst physicians were medical/clinical microbiologists at 47 %, followed by infectious disease physicians at 33 % and internal medicine practitioners at 17 %. Over 50 % of the respondents had appointments in academic hospitals, and 57 % had experience of ten years or more in the area of infection prevention and control.

The overall ranking of topics is outlined in Table 1. Microbial epidemiology/resistance was considered the highest priority, achieving a mean score of 8.9. This was followed by surveillance, 8.2, decolonisation/disinfection/antiseptics, 8.1 and organisational and behavioural change as well as specific HCAIs and settings at 7.9. The distribution of the scores for the specific key topics from Europe and beyond Europe is shown in Table 2. Interestingly, there was consensus across all continents that microbial resistance was the most important topic.

Table 1 Order and ranking score for key topics in infection prevention and control
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Table 2 Scores for specific key topics—Europe and World regions other than Europe
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Under the heading of microbial epidemiology/resistance, the control of highly resistant Gram-negative pathogens including those producing extended-spectrum β-lactamase enzymes had the highest score at 9.0—9.2. This was followed by multiresistant Gram-positive bacteria (8.4) and Clostridium difficile infection (7.9). Also under microbial epidemiology/resistance, the development of reliable, affordable and accessible rapid laboratory detection methods had a score of 8.8.

Under surveillance, the evaluation of computerised healthcare information systems for the early detection of outbreaks of HCAI, including multidrug-resistant pathogens was the top priority with a score of 8.3 followed by the standardisation of surveillance, including definitions at 8.1. Research on the effects of decolonisation of patients harbouring multidrug-resistant bacteria on infection rates was the top priority in the category of decolonisation/disinfection/antiseptics, with a score of 8.1. This was followed by studies on the effect of surface disinfectants (7.9) and investigations into the clinical effectiveness of antiseptic compounds (7.8). Regarding specific HCAI and certain settings, two areas achieved equal high priority, i.e., the development of protocols/checklists and new technologies to improve the prevention of surgical site infections and to prevent central line infections, both of which scored 7.9. These were followed by the development of scoring systems and new technologies to improve the diagnosis of ventilator-associated pneumonia.

In addition to scoring and prioritising key topics, participants were also invited to provide free comments, which ranged from remarks about the survey itself and about specific HCAI issues. The 49 comments included the need for support for infection prevention and control programmes in lower income countries, the role of the colonised healthcare worker in the spread of multidrug-resistant organisms and the need for protocols and interpretative guidelines for routine environmental sampling in preventing HCAI.

Differences existed when the scores are subdivided by European and non-European regions (Tables 2 and 3). For example, healthcare delivery factors scored significantly higher in Southeastern as compared to Northern Europe.

Table 3 Test for differences (Wilcoxon rank sum test) between Europe versus other regions and within Europe
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Discussion

Associated with the increased public awareness and burden on modern healthcare systems, efforts are underway locally, nationally and internationally to support the prevention and control of HCAIs and antimicrobial resistance. Increased numbers of scientific publications describing relevant clinical studies reflect this evolution [12, 13].

In this study of approximately 600 participants across five continents, microbial epidemiology and the control of multidrug-resistant bacteria, especially Gram-negative bacteria, had the highest priority for intervention, followed by better surveillance systems (early detection of outbreaks). Interestingly, scientific and practical issues regarding decolonisation/disinfection and antiseptic compounds are considered of high relevance today, which is in some contrast to their role a decade ago. These findings are helpful in highlighting what the consensus is amongst infection prevention and control practitioners on the key areas that need to be addressed in terms of informing key healthcare and political decision makers at local, national and international level. Also, differences between different regions within Europe and between Europe and other continents should specifically inform national and regional priority setting. This information may be helpful to further develop special programmes for HCAI control, keeping in mind that ‘one fits all’ solutions will not be a realistic approach [6].

Whilst the results from this survey are of interest, there are limitations to the study. As this was a voluntary survey and the participants were self-selected, we cannot validate how representative those who participated were, and whether or not they truly reflect the views and opinions of infection prevention experts and practitioners in their respective countries or disciplines. The relatively low response rate may add to this limitation. Also, we did not verify the qualifications or experience of the participants, and it may be that the results reflect the most enthusiastic individuals rather than key opinion leaders who did not allocate time to fill out the survey during the designated period. Whilst we did allow participants to enter free comments to highlight other important areas, the ESGNI Co-ordinating Study Group predetermined the topics and the subtopics. However, we felt that this was necessary to enable us to analyse the data in a practical and meaningful way. Whilst hand hygiene was not specifically addressed as a topic in its own right, its importance was underlined in comments. Infection control nurses were not specifically addressed, because they are not regular members of ESCMID.

In summary, the highest score was reached by the topic “microbial epidemiology/resistance”, followed by “surveillance” and “decolonisation/disinfection/antiseptic compounds”. Also, relevant insights were gained through individual comments. Altogether, well-organised and effective initiatives and measures in infection prevention and antimicrobial resistance control are required, and the commitment of resources may be guided to some extent by our findings. Finally, this survey represents a useful resource when discussions take place on determining priorities and the allocation of resources nationally and at European level, and the survey should probably be repeated at least every decade to assist in any review of those priorities.