Prevention of ventilator-associated pneumonia in intensive care units: an international online survey

  • Marie-Laurence Lambert1Email author,

    Affiliated with

    • Mercedes Palomar2, 3,

      Affiliated with

      • Antonella Agodi4,

        Affiliated with

        • Michael Hiesmayr5,

          Affiliated with

          • Alain Lepape6,

            Affiliated with

            • Anne Ingenbleek1,

              Affiliated with

              • Eduardo Palencia Herrejon7,

                Affiliated with

                • Stijn Blot8 and

                  Affiliated with

                  • Uwe Frank9

                    Affiliated with

                    Antimicrobial Resistance and Infection Control20132:9

                    DOI: 10.1186/2047-2994-2-9

                    Received: 25 January 2013

                    Accepted: 7 March 2013

                    Published: 26 March 2013

                    Abstract

                    Background

                    On average 7% of patients admitted to intensive-care units (ICUs) suffer from a potentially preventable ventilator-associated pneumonia (VAP). Our objective was to survey attitudes and practices of ICUs doctors in the field of VAP prevention.

                    Methods

                    A questionnaire was made available online in 6 languages from April, 1st to September 1st, 2012 and disseminated through international and national ICU societies. We investigated reported practices as regards (1) established clinical guidelines for VAP prevention, and (2) measurement of process and outcomes, under the assumption “if you cannot measure it, you cannot improve it”; as well as attitudes towards the implementation of a measurement system. Weighted estimations for Europe were computed based on countries for which at least 10 completed replies were available, using total country population as a weight. Data from other countries were pooled together. Detailed country-specific results are presented in an online additional file.

                    Results

                    A total of 1730 replies were received from 77 countries; 1281 from 16 countries were used to compute weighted European estimates, as follows: care for intubated patients, combined with a measure of compliance to this guideline at least once a year, was reported by 57% of the respondents (95% CI: 54–60) for hand hygiene, 28% (95% CI: 24–33) for systematic daily interruption of sedation and weaning protocol, and 27% (95%: 23–30) for oral care with chlorhexidine. Only 20% (95% CI: 17–22) were able to provide an estimation of outcome data (VAP rate) in their ICU, still 93% (95% CI: 91–94) agreed that “Monitoring of VAP-related measures stimulates quality improvement”. Results for 449 respondents from 61 countries not included in the European estimates are broadly comparable.

                    Conclusions

                    This study shows a low compliance with VAP prevention practices, as reported by ICU doctors in Europe and elsewhere, and identifies priorities for improvement.

                    Keywords

                    Healthcare associated infection Ventilator-associated pneumonia Patient safety Preventive measures Quality of care

                    Introduction

                    Ventilator-associated pneumonia (VAP) is a frequent and severe health-care associated infection. In Europe, pneumonia occur in 7.0% of patients staying at least 2 days in intensive care units (ICUs); 91% of these pneumonia are VAP [1]. The proportion of VAP which is preventable is debated [2] but there is no doubt that a serious potential for harm reduction does exist [3, 4] and VAP prevention is becoming a major patient safety issue. In the US for instance, VAP prevention has been proposed as a national safety goal [2].

                    VAP prevention requires clinical interventions (best practice guidelines) combined with non clinical interventions to ensure implementation and compliance with these guidelines.

                    Clinical interventions for VAP prevention fall in three categories [5]. The first, obvious one, is to limit exposure to mechanical ventilation by preferring non-mechanical ventilation when possible and limiting its duration when alternative options are not possible. Other prevention practices aim at reducing airways colonization (such as oral care decontamination using chlorhexidine [6]), or preventing aspiration [5] (e.g. by nursing in the semi-recumbent position, or maintaining a sufficient cuff pressure). Clinical interventions should be combined, in what is often called a “care bundle”. The precise content of VAP care bundle varies between guidelines [7, 8] because the number of items in a “bundle” should be limited, some prevention practices are controversial (e.g. selective digestive decontamination), [9] and recommending best practice regarding such measures requires compromise and pragmatism [8]. There is no universally accepted “VAP care bundle”. A study aiming at defining a “European care bundle” ranked VAP prevention measures by combining criteria such as the strength of the supporting evidence, ease of implementation, and expected impact [10]. The top 5 clinical interventions (we did not consider “trained staff” as a clinical intervention) were: 1) no ventilatory circuit change unless specifically indicated; 2) strict hand hygiene with alcohol especially before managing the airways; 3) daily sedation vacation and weaning protocol; 4) oral care with chlorhexidine; and 5) cuff pressure control at least every 24 hrs. It was beyond the scope of our study to assess the evidence behind each of these interventions, but none appears to be controversial.

                    Ensuring compliance with guidelines is a vast and complex field of research [1113]. Common to any improvement strategy is the need for measurement; this serves evaluation purposes, measurement can also be the intervention, or a major component of it [1416]. In a survey on infection control practices in the US, ICUs were only able to reduce heathcare-associated infection rates (including VAP), when they had a written policy, monitored compliance, and achieved a ≥95% compliance to all elements included in the local care bundle [11, 17]. Under the unchallenged assumption “if you cannot measure it, you cannot improve it” (Lord Kelvin, 1824-1907), we considered here that monitoring process (compliance to guidelines) and outcomes is a necessary, if not sufficient, component of any intervention aiming at decreasing VAP.

                    Accurate diagnosis of VAP is a challenge, because many conditions commonly encountered in critically ill patients – such as pulmonary oedema, pulmonary hemorrhage and acute respiratory distress syndrome, can mimic the signs and symptoms of pneumonia [5]. Clinical diagnosis leads to treatment decisions, its primary aim is to be accurate, and it cannot be entirely standardized. By contrast measurement need primarily to be reproducible to ensure comparability of data overtime and allow evaluation of trends. Standardization is essential. Criteria for diagnosis and criteria for recording, therefore do not necessarily overlap entirely. Guidelines and definitions of VAP for recording and reporting exist in Europe [18] and in the United States [19]. Despite some changes in the US, current case-definitions are still considered useful for internal quality improvement purposes [20].

                    Our objectives were to document, using a web-based survey (1) reported VAP prevention practices in ICUs (clinical practices, and measurement) and (2) attitudes towards the implementation of a measurement system. Our primary interest laid in providing estimates at European level, but we did not define exclusion criteria based on geographical location; on the other hand country-specific results can be used to steer prevention initiatives at country level.

                    Methods

                    Study population

                    Our target group was physicians working in ICUs. An ICU was defined as an unit meeting all the following criteria: provides facilities for invasive mechanical ventilation, and pump-controlled administration of infusion, functions 24 hours a day and 7 days a week, and there is at least one doctor immediately available at all times to deal with emergencies.

                    Questionnaire

                    We developed a questionnaire with 3 parts: 1) Characteristics of the respondent and her/his ICU, 2) VAP prevention practices (clinical, and measurement). For clinical practices we focused on the top 5 clinical components of the European VAP care bundle [10] and added a commonly recommended practice (head of bed elevation) [5]. For measurement, we included questions on measurement of process (compliance to prevention practices, average duration of intubation) and outcomes (measurement of VAP, definitions used for data collection – European, [18] or American, [19] and the ability to report selected indicators. 3) attitudes as regards the implementation of a data collection system, using a 5 point-Likert scale (1: strongly agree, 5: strongly disagree) [13, 21]. The questionnaire was kept very short to improve participation. It was first developed and pre-tested in English, then translated into German, Italian, Spanish, Portuguese and French by intensive care doctors and/or infection control practitioners, native speakers in the targeted language. Each translation had to be independently checked by at least another native speaker doctor. We used Limesurvey 2.0, an open source web survey application, to collect the data [22]. Participation was anonymous.

                    Dissemination to target group

                    The questionnaire was available online from April 1 to September 1, 2012. It was endorsed by the European Society of Intensive Care Medicine (ESICM), posted on their website, and the link e-mailed to all its members. We contacted national ESICM representatives and key opinion leaders and requested their support in disseminating the survey in their country. The survey was endorsed by national ICU societies in Austria, France, Belgium, the Netherlands, Italy, and Greece. It was e-mailed to all subscribers of REMI (Revista Electronica de Medicina Intensiva), [23] an electronic newsletter on intensive care medicine in Spanish distributed in Spain, Portugal, and Latin America.

                    Data analysis

                    Descriptive statistics were used to characterize the study sample. Using total country population (2012 United Nations estimates [24]) as the weight, we computed weighted European estimates including all countries which provided at least 10 completed replies. This arbitrary threshold was chosen as a compromise between the number of countries included in the European estimates, and precision of the estimation. Statistical software STATA 10 was used for the analyses (svy command for survey data for weighted estimates). Replies from the remaining countries, both European and non European, were simply pooled together. We choose to present uncommented, detailed country-specific results as Additional file 1, for use by national stakeholders.

                    Results

                    A total of 1730 completed replies from 77 different countries were submitted (Table 1). Characteristics of the respondents, and their setting, are presented in Table 2.
                    Table 1

                    Number of replies to the survey, by country

                     

                    Replies

                    %

                    European countries

                      

                    Spain

                    293

                    17%

                    France

                    251

                    15%

                    Italy

                    187

                    11%

                    Austria

                    130

                    8%

                    United Kingdom

                    115

                    7%

                    Germany

                    67

                    4%

                    Portugal

                    50

                    3%

                    Belgium

                    33

                    2%

                    Netherlands

                    31

                    2%

                    Switzerland

                    29

                    2%

                    Greece

                    23

                    1%

                    Romania

                    20

                    1%

                    Denmark

                    15

                    1%

                    Sweden

                    14

                    1%

                    Ireland

                    13

                    1%

                    Hungary

                    10

                    1%

                    Total European countries with at least 10 replies*

                    1281

                    74%

                    Other (18 different countries)

                    55

                    3%

                    Non European countries

                      

                    India

                    63

                    4%

                    Argentina

                    40

                    2%

                    Colombia

                    31

                    2%

                    Mexico

                    31

                    2%

                    Australia

                    23

                    1%

                    Peru

                    23

                    1%

                    Brazil

                    21

                    1%

                    Ecuador

                    13

                    1%

                    Chile

                    12

                    1%

                    Turkey**

                    12

                    1%

                    United States

                    12

                    1%

                    Saudi Arabia

                    11

                    1%

                    United Arab Emirates

                    11

                    1%

                    Venezuela

                    11

                    1%

                    Other (29 different countries)

                    80

                    5%

                    Survey - total

                    1730

                    100%

                    * Used for European weighted estimates.

                    ** Considered as non European as majority of population does not live in Europe.

                    Table 2

                    Characteristics of the respondents, and of their setting

                    Respondent

                    Weighted estimates for Europe (respondents from 16 countries with >=10 replies)

                    Other respondents (61 countries)

                     

                    N=1281

                    95% CI

                    N=449

                    95% CI

                    Years working in ICU (mean)

                    12.8

                    12.2

                    13.3

                    12.9

                    12.1

                    13.6

                    Admissions per year in their ICU (mean)

                    1006

                    914

                    1098

                    900

                    787

                    1013

                    N beds in ICU (mean)

                    16

                    15

                    17

                    16

                    15.4

                    17.3

                     

                    %*

                      

                    N

                    %

                      

                    Gender (females)

                    28

                    25

                    31

                    82

                    18

                    15

                    22

                    Working in hospital with > 1000 beds

                    17

                    14

                    20

                    18

                    4

                    2

                    6

                    Working in hospital with 300–1000 beds

                    55

                    52

                    56

                    145

                    33

                    28

                    37

                    Working in hospital <300 beds

                    28

                    26

                    31

                    282

                    63

                    58

                    67

                    * Absolute numbers are not reported because percentages are weighted estimates.

                    Weighted European estimates are based on 1281 respondents from the 16 countries from which at least 10 completed replies were available.

                    VAP prevention practices are presented in Table 3 (clinical practices) and Table 4 (measurements).
                    Table 3

                    VAP prevention: clinical practices, as reported by ICU doctors

                    Clinical practice

                    Weighted estimates for Europe (respondents from 16 countries with >=10 replies)

                    Other respondents (61 countries)

                     

                    N=1281

                    N=449

                     

                    %*

                    95% CI

                    N

                    %

                    95% CI

                    In my ICU, hand hygiene is done with alcohol hand rub, always, or most of the time

                    95

                    94

                    97

                    395

                    88

                    85

                    91

                    In my ICU, there are written guidelines for VAP prevention

                    65

                    62

                    69

                    282

                    63

                    58

                    67

                    Guidelines developed locally

                    33

                    30

                    36

                    162

                    36

                    32

                    41

                    Guidelines developed nationally

                    31

                    28

                    34

                    117

                    26

                    22

                    30

                    In my ICU, care for intubated patients includes…

                           

                    No ventilatory circuit changes unless specifically indicated

                    69

                    66

                    72

                    371

                    83

                    79

                    86

                    Strict hand hygiene using alcohol, especially before managing the airways

                    83

                    80

                    86

                    364

                    81

                    77

                    85

                    Systematic daily interruption of sedation and weaning protocol

                    49

                    46

                    53

                    285

                    63

                    59

                    68

                    Oral care with chlorhexidine

                    70

                    67

                    73

                    302

                    67

                    63

                    72

                    Cuff pressure control at least every 24 hours

                    83

                    81

                    85

                    347

                    77

                    73

                    81

                    Head of bed elevation

                    96

                    94

                    97

                    442

                    98

                    97

                    100

                    * Absolute numbers are not reported because percentages are weighted estimates.

                    Table 4

                    VAP prevention: measurements, as reported by ICU doctors

                    Measurements

                    Weighted estimates for Europe (respondents from 16 countries with >=10 replies)

                    Other respondents (61 countries)

                     

                    N=1281

                    N=449

                     

                    %*

                    95% CI

                    N

                    %

                    95% CI

                    Measurement of compliance at least once a year

                           

                    Hand hygiene recommendations

                    57

                    54

                    60

                    265

                    60

                    54

                    64

                    Systematic daily interruption of sedation and weaning protocol

                    28

                    24

                    33

                    102

                    23

                    19

                    27

                    Oral care with chlorhexidine

                    27

                    23

                    30

                    126

                    28

                    24

                    32

                    “In my ICU, there is a written definition of VAP for data collection”

                    50

                    47

                    54

                    286

                    64

                    59

                    68

                    YES- European guidelines

                    26

                    23

                    29

                    37

                    8

                    6

                    11

                    YES- CDC guidelines

                    12

                    10

                    15

                    206

                    46

                    41

                    51

                    “In my ICU, we count and record, routinely…” (% saying “yes”)

                           

                    VAP

                    55

                    51

                    58

                    287

                    64

                    59

                    68

                    Intubation-days

                    81

                    78

                    84

                    364

                    81

                    74

                    85

                    Intubated patients

                    90

                    88

                    92

                    367

                    82

                    78

                    85

                    Please provide, if possible, the following data for your ICU - for part or all 2011 (% providing data)

                           

                    VAP/ 1000 ventilation-days

                    20

                    17

                    22

                    113

                    25

                    21

                    29

                    Mean duration of intubation for intubated patients (days)

                    27

                    25

                    30

                    148

                    33

                    29

                    37

                    Proportion of intubated patients

                    38

                    35

                    41

                    178

                    40

                    35

                    44

                    “Clinical staff in my ICU is aware of VAP-related measures, and their trends” (% agree strongly / agree)

                    53

                    50

                    56

                    298

                    66

                    62

                    71

                    * Absolute numbers are not reported because percentages are weighted estimates.

                    Attitudes towards the implementation of a VAP measurement system are presented in Table 5.
                    Table 5

                    Attitudes towards the implementation of a measurement system of infections in ICUs

                     

                    Weighted estimates for Europe (respondents from 16 countries with >=10 replies)

                    Other respondants (66 countries)

                     

                    N=1281

                    N=449

                     

                    Agree strongly/ agree

                    Disagree/ disagree strongly

                    Agree strongly/ agree

                    Disagree/ disagree strongly

                     

                    %

                    95% CI

                    %

                    95% CI

                    %

                    95% CI

                    %

                    95% CI

                        

                    To what extent do you agree with the following comments

                    If you cannot measure it, you cannot improve it

                    83

                    80

                    85

                    11

                    9

                    13

                    84

                    80

                    87

                    11

                    8

                    14

                    Monitoring of VAP related measures stimulates quality improvement

                    93

                    91

                    94

                    2

                    1

                    3

                    97

                    94

                    98

                    1

                    0

                    3

                    VAP-related measures in my ICU (if any) are reliable

                    54

                    51

                    58

                    12

                    10

                    15

                    66

                    61

                    70

                    8

                    6

                    11

                    I am willing to implement, or support, a VAP data collection system

                    84

                    81

                    86

                    4

                    3

                    6

                    92

                    89

                    94

                    1

                    0

                    3

                    Clinical diagnosis of VAP is difficult: this makes measurement systems unreliable

                    46

                    43

                    50

                    32

                    29

                    36

                    43

                    38

                    47

                    36

                    32

                    41

                    There is a difference between a definition of VAP for reporting, and a diagnosis of VAP for treatment

                    45

                    42

                    49

                    32

                    28

                    35

                    46

                    41

                    50

                    30

                    26

                    35

                    Please indicate what actions would facilitate the implementation of a measurement system of infections in ICUs

                    Timely feed-back of data at ICU level

                    92

                    90

                    94

                    1

                    1

                    2

                    96

                    93

                    97

                    0

                    0

                    2

                    Administrative support

                    88

                    86

                    90

                    2

                    1

                    3

                    95

                    92

                    97

                    1

                    0

                    2

                    Dedicated software / IT resources

                    91

                    89

                    93

                    2

                    1

                    3

                    92

                    89

                    94

                    0

                    0

                    2

                    Reliable data

                    95

                    93

                    96

                    1

                    0

                    2

                    96

                    94

                    98

                    0

                    0

                    1

                    Discussion

                    Key results

                    This is, to our knowledge, the first international survey assessing VAP prevention practices – (clinical, and measurement) – among ICUs doctors. Participation was large, and almost two thirds of respondents reported the existence of written VAP prevention guidelines in their ICU - pointing out the interest in, and awareness of the problem. If we combine the good clinical practice, AND measuring compliance to this practice at least once a year (a very pragmatic objective), this was reported by 57% (hand hygiene), 29% (daily interruption of sedation) and 26% (oral care with chlorhexidine) of the participants to this survey (European estimates). Interestingly, “head of bed elevation” - a practice ranked very low in the “European care bundle” because it was perceived as difficult to implement - was mentioned by 96% of the respondents; this clinical practice was known by 85% of European nurses participating in a knowledge test about VAP prevention practices [25].

                    As regards measurement of outcomes, European estimates show that only 54% count and record the number of VAP on a routine basis; and only 20% were able to provide data for their ICU on the main indicator used to monitor VAP - (VAP/1000 intubation-days). In contrast with these low proportions 93% agreed that “monitoring of VAP-related measures stimulates quality improvement” and 84% said they were willing to implement, or support, a VAP data collection system. They expressed some distrust as regards the data (46% agreed with the statement “clinical diagnosis of VAP is difficult; this makes measurement unreliable”), on the other hand, only 50% were aware of a standardized case definition for VAP recording in their ICU; and only 45% understood the difference between a definition of VAP for recording, and a diagnosis of VAP. Overall, 95% of respondents agreed that reliable data would facilitate the implementation of a measurement system.

                    These European estimates mask large difference between countries. For example oral care with chlorhexidine was reported by 55% (139/251) of the respondents in France, and by 94% (276/293) in Spain. Respondents saying yes to the question “in my ICU, we count and record VAP on a routine basis” were 50% (57/115) in the UK, and 74% (218/293) in Spain. Daily sedation vacation and weaning protocol were reported by 81% (93/115) in the UK, and by 35% (66/187) in Italy (see country-specific data, as Additional file 1).

                    Results from the 449 respondents not included in the European estimates are surprisingly similar to those of the European estimates.

                    Strengths and Limitations

                    This survey has several limitations. First, we cannot claim that participants represent a random sample of ICU clinicians in Europe nor in their own country. Some categories of ICU doctors are likely to be overrepresented, such as members of ICU national, or international societies. These might be better informed, and apply VAP prevention guidelines more than the average clinician. The list of VAP prevention measures we used as a reference for good practices guidelines [10] could be criticized on several grounds, e.g. it does not include subglottic secretions drainage [26]. Our dissemination strategy obviously worked better in some countries than others. Another limitation is that some questions in the questionnaire apply to the individual physician and others to the ICU (“in my ICU, care for intubated patients includes…) but the online questionnaire did not include questions allowing for the identification of the ICU, in order to preserve the anonymity of the respondents.

                    Respondents not included in the European estimates represent a very heterogeneous population with no clear geographical basis. We nevertheless considered it worthwhile to pool these results, because together these doctors are responsible for a large number of patients, and these data have identified weaknesses broadly similar to those observed in the European estimates.

                    Clearly, it cannot be concluded from a doctor’s reporting of a clinical practice in her/his setting, that this practice is used all the time for every patient who needs it: self-reports mainly provide information regarding clinicians’ knowledge of guideline recommendations, but they are subject to bias – overestimation – and should not be used as the sole measure of guideline adherence [27]. Measuring compliance to guidelines at local level once a year appears as an absolute minimum. We did not ask details on the methods used to measure compliance. This is not necessarily easy, for instance detailed guidelines exist for measuring compliance to hand hygiene recommendations; [28] and oral care in ventilated patients is a complex procedure that might require a check list [29].

                    It was not among the objectives of this survey to collect data on VAP incidence rate in ICUs – there are much better sources for this – e.g. surveillance data for Europe [1]. Rather we wanted to investigate the knowledge doctors had of the rates in their units. However data provided on VAP rates (not shown) are in the expected range as reported in surveillance networks [1], giving some validity to our results.

                    Interpretation

                    The large participation to this survey reflects the interest of the ICU community in the issue of VAP prevention. To the extent that the selection bias, and the reporting bias in our results lead to overestimating VAP prevention practices in ICUs, weaknesses identified appear robust enough as to support targeted interventions for improvement. The priority for improving care of intubated patients is promoting the clinical practices with the lowest reported use (daily sedation vacation, and weaning protocols, oral care with chlorhexidine, and no ventilatory circuit change unless specifically indicated). Improving knowledge of clinical guidelines is far from sufficient to improve practices [25, 30] but it is a prerequisite. ICUs doctors overwhelmingly agree that monitoring of VAP-related measures stimulates quality improvement but very few do it, although most are willing to do it. They could be helped to do so by learning how to produce reliable data (standardized case-definitions, methods for measuring compliance) with real-time feed-back at the ICU level; so that clinical staff could monitor their own trends over time. A compromise needs to be found between time-consuming data collection, and usefulness of data. Additional resources (human resources, information technology) might help, but some very simple measures can be implemented with minimal input, e.g. in some ICUs a panel with the number of days since last ICU-acquired infection (including VAP) is displayed on the board and updated daily (personal observations in Scotland, MLL). This study did not consider the issue of surveillance and reporting of outcome indicators at regional or national level, nor the merits (or otherwise) of evaluation of performance and feed-back, based on benchmarking (e.g. comparisons between units). Specific priorities might differ between countries.

                    Conclusions

                    This survey has documented a large potential for improvement in clinical and non-clinical practices aimed at preventing VAP in ICUs. Some results, such as a large agreement of the respondents that data collection is essential – “if you cannot measure it, you cannot improve it” - extend beyond the issue of VAP prevention. Promoting the implementation of guidelines for VAP prevention needs to be done together with promoting the measurement of compliance to these guidelines and measurement of outcomes as a tool for improvement, keeping data collection systems at ICU level as simple as possible: what is important is usefulness, not perfection [31].

                    Declarations

                    Acknowledgments

                    We are grateful to the following collaborating partners for their contribution to the project: Afonso Elsa, Antonelli Massimo, Aragao Irene, Brun-Buisson Christian, Cardoso Teresa, Catry Boudewijn, Cunha Andreia, De Boom Dominique, François Guy, Hoste Eric, Kaier Klaus, Koulenti Despoina, Mura Ida, Muzlovic Igor, Popa Mircea Ioan, Preiser Charles, Rello Jordi, Savey Anne, Schouten Jeroen, Stevens Alan, Tamowicz Barbara, Via Gabriele, Zapletal Bernhard.

                    Data sharing

                    Data are freely available and have been deposited in the Dryad Digital Repository http://​datadryad.​org doi:http://​10.​5061/​dryad.​q1d7f Further use and exploitation of these data is encouraged.

                    Funding

                    This study was supported by the European Commission (Project IMPLEMENT , commissioned by Directorate General for Health and Consumer Protection (DG SANCO), Grant Agreement N° 2009-11-07; (http://​www.​eu-implement.​info).

                    The funding source had no role in the study design, collection, analysis, and interpretation of data, nor in the decision to submit the manuscript.

                    Authors’ Affiliations

                    (1)
                    Healthcare associated infections unit, Scientific Institute of Public Health
                    (2)
                    Intensive care department, Hospital Vall d’Hebron
                    (3)
                    Universitat Autonoma de Barcelona
                    (4)
                    Department GF Ingrassia, University of Catania
                    (5)
                    Department Anaesthesia, General Intensive Care and Pain Control, Medical University of Vienna
                    (6)
                    Department Anaesthesia, General Intensive Care, University hospital
                    (7)
                    Intensive Care department, Hospital Universitario “Infanta Leonor”
                    (8)
                    Department of Internal Medicine, Ghent University
                    (9)
                    Infectious diseases department, University hospital

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                    This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://​creativecommons.​org/​licenses/​by/​2.​0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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