Abstract
Rationale
Early detection, standardized therapy, adequate infrastructure, and strategies for quality improvement should constitute essential components of every hospital’s sepsis plan.
Objectives
To investigate the extent to which recommendations from the sepsis guidelines are implemented and the availability of infrastructure for the care of patients with sepsis in acute-care hospitals.
Methods
A multidisciplinary cross-sectional questionnaire was used to investigate sepsis care in hospitals. This included the use of sepsis definitions, the implementation of sepsis guideline recommendations, diagnostic and therapeutic infrastructure, antibiotic stewardship, and quality improvement initiatives (QIIs) in hospitals.
Measurements and Main Results
A total of 1,023 hospitals in 69 countries were included. Most of them, 835 (81.6%), were in Europe. Sepsis screening was used in 54.2% of emergency departments (EDs), 47.9% of wards, and 61.7% of ICUs. Sepsis management was standardized in 57.3% of EDs, 45.2% of wards, and 70.7% of ICUs. The implementation of comprehensive QIIs was associated with increased screening (EDs, +33.3%; wards, +44.4%; ICUs, +23.8% absolute difference) and increased standardized sepsis management (EDs, +33.6%; wards, +40.0%; ICUs, +17.7% absolute difference) compared with hospitals without QIIs. A total of 9.8% of hospitals had implemented ongoing QIIs, and 4.6% had invested in sepsis programs.
Conclusions
The findings indicate that there is considerable room for improvement in a large number of mainly European hospitals, particularly with regard to early identification and standardized management of sepsis, the availability of guidelines, diagnostic and therapeutic infrastructure, and the implementation of QIIs. Further efforts are required to implement a more comprehensive and appropriate quality of care.
Keywords: sepsis screening, sepsis management, standard of care, quality of care, sepsis programs
At a Glance Commentary
Scientific Knowledge on the Subject
There are few data on the implementation of guideline recommendations and infrastructure for the care of patients with sepsis in hospitals, especially in Europe.
What This Study Adds to the Field
This study investigated for the first time the implementation of guideline recommendations and infrastructure for the care of patients with sepsis in a large sample of mainly European hospitals.
The incidence of sepsis is high, with almost 49 million new cases and 11 million deaths worldwide per year (1). International guidelines strongly recommend routine sepsis screening in acutely ill patients at high risk and the application of standard operating procedures for sepsis treatment when indicated (2). In recent years, there has been international recognition of the need for hospital facilities to improve sepsis care. This is recognized by the seventh World Health Assembly resolution on “Improving the prevention, diagnosis, and management of sepsis” (Resolution 70.7) in 2017, which encouraged “Member States to define and implement standards and established guidelines, infrastructure, laboratory capacity, strategies, and tools for identifying, reducing incidence of, and morbidity and mortality due to sepsis” (3) and by the statement of the G7 Health Ministers in May 2022 to intensify efforts to strengthen early detection, diagnosis, and therapy of sepsis and to boost the implementation of the World Health Assembly 70.7 Resolution (4). One question is whether existing hospital facilities are ready to reach these goals. This would require the delivery to state authorities a real mapping of the existing facilities, including infrastructure, available personnel, and bundles of sepsis management to increase awareness of the necessary corrective actions.
The objective of this study was to investigate the implementation of sepsis guideline recommendations and the availability of infrastructure for the care of patients with sepsis in pivotal hospital departments in Europe and other regions. Some of the results of this study have been previously reported in the form of abstracts or conference contributions (5–18). Some of the results of these studies have been previously reported in the form of a preprint (Lancet, 2023 Aug 15; http://dx.doi.org/10.2139/ssrn.4538229).
Methods
The European Sepsis Care Survey (ESCS) was conducted to investigate the current status of sepsis care in hospitals. The ESCS was addressed to healthcare professionals working in different hospital settings, mostly in Europe, and tried to investigate the implementation of basic principles of sepsis recognition and management in routine clinical practice.
Study Design, Harmonization, and Pretesting
The ESCS, a cross-sectional questionnaire, was designed and harmonized by a multiprofessional steering committee led by the European Sepsis Alliance and peer-reviewed by the scientific committees of four European professional scientific societies (Table E1 in the online supplement). The survey included 94 questions, including overarching questions and concerning separate sections for the emergency departments (EDs), wards, and ICUs (see online supplement for the full survey).
The main focus of interest was the use of sepsis definitions and the implementation of Surviving Sepsis campaign guidelines, including sepsis screening for early recognition and standardized sepsis management, including standard operating procedures for management and quality improvement programs (2). Quality improvement initiatives (QIIs) are programs that include meetings, case reviews, informational material, and peer reviews with the aim to improve the quality of sepsis care.
A second focus of interest was infrastructure and resources for the care of patients with sepsis. This included the presence of medical emergency teams for the identification and evaluation of critically ill patients, the availability of imaging for the detection of the source of infection, the accessibility of microbiological diagnostic services, and the availability of surgical procedures for source control. The use of fluids for hemodynamic resuscitation, the implementation of antimicrobial guidelines or recommendations for antiinfective treatment, and the establishment of antibiotic stewardship teams were also identified as essential therapeutic and structural features.
The survey was available in English, German, Polish, Romanian, Russian, and Turkish. Technical and content-related pretesting was conducted by steering committee members and national coordinators. The study protocol received ethical approval from the ethics committee of University Medicine Greifswald, Germany (BB 124/21), where data are stored and processed. In all other countries, the study was approved per national legislation. The study complies with the EQUATOR (Enhancing the Quality and Transparency of Health Research) network reporting guidelines, CHERRIES (Checklist for Reporting Results of Internet E-Surveys) (19), and CROSS (Checklist for Reporting of Survey Studies) (20) and was registered at clinicaltrials.gov (identifier NCT05059808).
Sampling Strategy, Technical Realization, and Statistical Analysis
The ESCS was conducted between August 2021 and June 2022. The steering committee of the ESCS invited national coordinators from 26 countries and 8 international scientific societies. The national coordinators were tasked to invite hospitals in their respective countries in a way that was as representative as possible, taking into account the distinction between teaching and nonteaching hospitals, as well as tertiary and nontertiary hospitals. Participation was encouraged by calls from the endorsing scientific societies (see online supplement for further details regarding the recruitment strategies in each country). Participants self-registered or were registered by the national coordinators. Following an initial verification of the hospital at which the participant was employed, an invitation email was sent to the individual, containing a unique link to enable web-based participation. To prevent the inclusion of redundant or duplicate data, a single authorized representative from each hospital was invited to respond to all queries. In the event that the designated individual was unable to address all queries, other personnel from relevant departments (e.g., ED, inpatient wards, ICU, or microbiological laboratory) were consulted and invited to respond. The survey was conducted online using the survey software LamaPoll (platin version; Lamano GmbH and Co KG), which meets the requirements of the European Union General Data Protection Regulation and is certified by the Deutsches Institut für Normung ISO 27001 standard.
Hospitals were grouped in five regions: Northern, Eastern, Southern, and Western Europe and the rest of the world (i.e., not Europe), including Asia, Africa, and Central and South America according to the definition of United Nations M49 standard regions (21). Because of the well-known differences between hospitals in terms of their numbers of beds and different types, hospitals were classified according to the number of beds available, differentiating between 0–250 beds, 251–500 beds, 501–750 beds, 751–1,000 beds, and more than 1,000 beds. Additionally, hospitals were grouped according to their type, based on the classification provided by the participants. This resulted in three main categories: university or training hospitals, general or community hospitals, and independent or private hospitals. These findings are presented in Table E6 and Figure E7. General measures and infrastructure were analyzed for the entire hospital. Given the distinct organizational structures observed in the EDs, wards, and ICUs, a separate analysis was performed for each of these units.
With regard to sepsis screening and standardized sepsis management, we explored the implementation (i.e., yes/no) and specified the individual criteria used for recognition and measures for treatment. As recommended in the Surviving Sepsis campaign guidelines, QIIs and programs were analyzed in terms of implementation, scope, and funding. In the area of essential infrastructure, we investigated whether: 1) microbiological laboratories were able to incubate and analyze blood cultures and report the results, 2) imaging (computed tomography or magnetic resonance imaging) was used to identify the source of infection, and 3) surgery for source control was available on a 24/7 (i.e., service unlimited in time) basis. Data were analyzed using SPSS software (version 26.0; IBM). Only questionnaires with definitive or assignable answers (e.g., no/yes, specific criteria or measures) were included in the analysis. The results are presented as numbers and proportions with 95% CIs. The χ2 test was used to calculate P values with a significance level (α) lower than 0.05. Because of the multiple comparisons, a Bonferroni correction was performed. Uncorrected and corrected P values are presented in the tables. To date, there is a paucity of data regarding the optimal rates or levels of standardized screening and sepsis management in hospitals. Therefore, a comparative analysis was conducted between hospitals with hospital-wide QIIs across the ED, all wards, and ICUs and those within each of the regions. The performance gap between the two groups was calculated as the absolute difference.
Results
Participants from 1,294 hospitals registered for the survey. After excluding incomplete responses and duplicates (n = 271; 20.9%), 1,023 responses (response rate, 79.1%) from individual hospitals from 69 countries were included in this convenience sample. Hospitals included in the analyses were mainly from Western Europe (n = 335; 32.7%), Eastern Europe (n = 215; 21.0%), Southern Europe (n = 185; 18.1%), and Northern Europe (n = 100; 9.8%). A smaller group of hospitals outside Europe was also included (Figure 1 and Table E5). In total, general hospitals constituted 56.5% of the sample (n = 578), university hospitals 35.7% (n = 365), and private hospitals 7.8% (n = 80). The responses related to the wards were primarily from medical and surgical wards, and the statements relevant to ICUs stemmed primarily from interdisciplinary ICUs (Tables E8 and E9).
Figure 1.
Participating countries and numbers of hospitals in the different regions sampled (see Table E5 for detailed information).
Use of Sepsis Definitions
Most hospitals (45.4%; 95% CI, 42.3%–48.5%) reported using the Sepsis-3 definition (Table 1). The Sepsis-3 criteria were used more often in Northern Europe (48.0%; 95% CI, 37.9%–58.2%) and Southern Europe (53.5%, 95% CI, 46.0%–60.9%) than in Eastern Europe (39.5%; 95% CI, 33.0%–46.4%) and Western Europe (43.0%; 95% CI, 37.6%–48.5%). Sepsis-1 was used in 24.5% (95% CI, 21.9%–27.3%) of hospitals and more commonly in Eastern Europe (37.7%; 95% CI, 31.2%–44.5%). Sepsis-1 and Sepsis-3 criteria were used together in 23.2% (95% CI, 20.6%–25.9%) of hospitals. A smaller proportion of hospitals (6.9%; 95% CI, 5.5%–8.7%) used other criteria or had no definition for sepsis. Sepsis-3 was more frequently used in university hospitals (51.0%; 95% CI, 45.7%–56.2%) than in general hospitals (42.0%; 95% CI, 38.0%–46.2%) and more often in hospitals with more than 750 beds (Table 1).
Table 1.
Use of Sepsis Definitions in Different Regions and Hospital Sizes and Types
| No. of Hospitals | Sepsis-1 Used | Sepsis-3 Used | Sepsis-1 and Sepsis-3 Used | Any Other Definition or No Definition Used | |
|---|---|---|---|---|---|
| All hospitals | 1,023 | 24.5% (21.9%–27.3%) | 45.4% (42.3%–48.5%) | 23.2% (20.6%–25.9%) | 6.9% (5.5%–8.7%) |
| Region | |||||
| Northern Europe | 100 | 18.0% (11.0%–26.9%) | 48.0% (37.9%–58.2%) | 10.0% (4.9%–17.6%) | 24.0% (16.0%–33.6%) |
| Eastern Europe | 215 | 37.7% (31.2%–44.5%) | 39.5% (33.0%–46.4%) | 17.2% (12.4%–22.9%) | 5.6% (2.9%–9.5%) |
| Southern Europe | 185 | 22.7% (16.9%–29.4%) | 53.5% (46.0%–60.9%) | 20.0% (14.5%–26.5%) | 3.8% (1.5%–7.6%) |
| Western Europe | 335 | 18.2% (14.2%–22.8%) | 43.0% (37.6%–48.5%) | 33.4% (28.4%–38.8%) | 5.4% (3.2%–8.4%) |
| Other regions | 188 | 26.1% (19.9%–33.0%) | 46.8% (39.5%–54.2%) | 21.8% (16.1%–28.4%) | 5.3% (2.6%–9.6%) |
| Hospital size | |||||
| 0–250 beds | 295 | 29.8% (24.7%–35.4%) | 40.7% (35.0%–46.5%) | 24.4% (19.6%–29.7%) | 5.1% (2.9%–8.2%) |
| 251–500 beds | 298 | 25.8% (21.0%–31.2%) | 43.0% (37.3%–48.8%) | 22.8% (18.2%–28.0%) | 8.4% (5.5%–12.1%) |
| 501–750 beds | 157 | 22.3% (16.0%–29.6%) | 47.1% (39.1%–55.2%) | 22.3% (16.0%–29.6%) | 8.3% (4.5%–13.7%) |
| 751–1,000 beds | 133 | 17.3% (11.3%–24.8%) | 54.1% (45.3%–62.8%) | 21.8% (15.1%–29.8%) | 6.8% (3.1%–12.5%) |
| >1,000 beds | 140 | 20.0% (13.7%–27.6%) | 50.0% (41.4%–58.6%) | 23.6% (16.8%–31.5%) | 6.4% (3.0%–11.9%) |
| Hospital type | |||||
| General hospitals | 578 | 27.7% (24.1%–31.5%) | 42.0% (38.0%–46.2%) | 23.0% (19.6%–26.7%) | 7.3% (5.3%–9.7%) |
| University hospitals | 365 | 19.5% (15.5%–23.9%) | 51.0% (45.7%–56.2%) | 22.7% (18.5%–27.4%) | 6.8% (4.5%–9.9%) |
| Independent hospitals | 80 | 25.0% (16.0%–35.9%) | 43.8% (32.7%–55.3%) | 26.3% (17.0%–37.3%) | 5.0% (1.4%–12.3%) |
Data in parentheses are 95% CIs. “Sepsis-1” refers to the systemic inflammatory response syndrome criteria due to infection. “Sepsis-3” refers to new organ failure as evidenced by an increase in Sequential Organ Failure Assessment score by ≥2 due to infection.
Adherence to the Surviving Sepsis Campaign Guideline Recommendations
Sepsis Screening
Standardized sepsis screening (see online supplement for definitions) as a measure for early sepsis identification was used in 54.2% (95% CI, 50.6%–57.7%) of EDs, 47.9% (95% CI, 44.5%–51.3%) of wards, and 61.7% (95% CI, 58.4%–65.0%) of ICUs. There were significant differences in sepsis screening between regions (P < 0.001). Screening occurred more frequently in EDs and wards in Northern Europe than in the rest of Europe (Figure 2). There were no statistically significant differences between hospitals of different sizes or between general, university, and private hospitals (Tables E10–E12). Screening was done daily in 51.0% (95% CI, 46.0%–55.9%) of wards and 75.8% (95% CI, 71.9%–79.4%) of ICUs and less frequently or only on demand in the remaining wards and ICUs (Table E13). In EDs and wards with standardized sepsis screening practices, the most common screening criteria were respiratory rate (EDs, 89.8%; wards, 85.0%), blood pressure (EDs, 88.6%; wards, 83.0%), temperature (EDs, 87.2%; wards, 87.2%), heart rate (EDs, 84.6%; wards, 83.5%), and mental alterations (EDs, 86.5%; wards, 81.0%). Lactate measurement was used for screening in 77.9% of EDs and 61.8% of wards. In ICUs, blood pressure (92.3%) temperature (91.9%), lactate (89.8%), respiratory rate (89.4%), and mental alterations (89.3%) were the most common criteria for sepsis, followed by heart rate (88.7%) and organ dysfunction (88.5%). See Table E13 for details about the criteria for sepsis screening including biomarkers and scores.
Figure 2.
Screening for sepsis in different regions: proportions of screening in emergency departments, on wards, and in ICUs. The blue bars show the proportions of screening in the different regions. The green line represents the level of screening in emergency departments, wards, and ICUs in all hospitals that have a quality improvement initiative (QII) on a regular basis. The 95% CIs of hospitals with QIIs are displayed as green dotted lines. The absolute differences between hospitals with QIIs and hospitals in each region are displayed in gray (see Figure 5).
The complete set of four Systemic Inflammatory Response Syndrome criteria was used in 56.3% of EDs and 63.1% of ICUs in hospitals that applied the Sepsis-1 definition. A greater number of hospitals used a reduced set of Systemic Inflammatory Response Syndrome criteria. Hospitals that used the Sepsis-3 definition were more likely to use the quick Sequential Organ Failure Assessment and Sequential Organ Failure Assessment scores, particularly within the ICUs (82.5% vs. 51.4% in hospitals that used the Sepsis-1 definition) (see Table E13). Early warning scores such as the New Early Warning Score or Modified Early Warning Score were used in 31.1% of EDs, 38.2% of wards, and 19.6% of ICUs. A total of 79.6% (95% CI, 70.3%–87.1%) of respondents from hospitals in Northern Europe stated that medical emergency teams (METs) who help to identify critically ill patients early were implemented in their hospitals. In all other regions, the availability of METs was significantly lower (Table E14). In hospitals with 0–250 beds, METs were available in 43.3% (95% CI, 37.5%–49.2%), compared with 58.8% (95% CI, 49.8%–67.3%) in hospitals with more than 1,000 beds. University hospitals (58.6%; 95% CI, 53.3%–63.8%) had METs more often than general hospitals (47.5%; 95% CI, 43.3%–51.6%) (see Table E14).
Standardized Sepsis Management
Protocols for standardized sepsis management (see online supplement for definitions) were reported to be available in 57.3% (95% CI, 53.7%–60.8%) of EDs, 45.2% (95% CI, 41.7%–48.6%) of wards, and 70.7% (95% CI, 67.5%–73.8%) of ICUs. There were significant differences in standardized sepsis management in EDs in different regions (Figure 3) but not between hospitals of different sizes (Tables E15–E17). The actions in hospitals with standardized sepsis management are displayed in Table 2.
Figure 3.
Standardized sepsis management in different regions: proportions of standardized sepsis management in emergency departments, on wards, and in ICUs. The brown bars show the proportions of standardized sepsis management in the different regions. The green line represents the level of standardized sepsis management in emergency departments, wards, and ICUs in all hospitals that have a quality improvement initiative (QII) on a regular basis. The 95% CIs of hospitals with QII are displayed as green dotted lines. The absolute differences between hospitals with QIIs and hospitals in each region are displayed in gray (see Figure 5).
Table 2.
Actions in Hospitals with Standardized Sepsis Management
| Action | Emergency Departments (n = 444) | Wards (n = 374) | ICUs (n = 589) |
|---|---|---|---|
| Surviving Sepsis campaign bundle | |||
| Measuring lactate level | 93.2% (90.5%–95.4%) | 81.6% (77.2%–85.4%) | 96.4% (94.6%–97.8%) |
| Obtaining blood cultures before administration of antibiotics | 97.3% (95.3%–98.6%) | 97.1% (94.8%–98.5%) | 98.0% (96.5%–98.9%) |
| Administering broad-spectrum antibiotics | 91.0% (87.9%–93.5%) | 93.6% (90.6%–95.8%) | 96.8% (95.0%–98.0%) |
| Beginning rapid administration of crystalloid* | 91.2% (88.2%–93.7%) | 88.8% (85.1%–91.8%) | 94.2% (92.0%–96.0%) |
| Applying vasopressors to maintain MAP ⩾65 mm Hg† | 81.8% (77.8%–85.2%) | 65.8% (60.7%–70.6%) | 96.9% (95.2%–98.2%) |
| Organ dysfunction | |||
| Blood testing‡ | 93.7% (91.0%–95.8%) | 91.4% (88.1%–94.1%) | 96.9% (95.2%–98.2%) |
| Catheterization/urine output measurement | 72.3% (67.9%–76.4%) | 74.3% (69.6%–78.7%) | 90.3% (87.6%–92.6%) |
| SOFA score | 55.4% (50.6%–60.1%) | 43.3% (38.2%–48.5%) | 77.8% (74.2%–81.1%) |
| Identification of source | |||
| Computed tomography | 38.1% (33.5%–42.8%) | 39.0% (34.1%–44.2%) | 50.1% (46.0%–54.2%) |
| Ultrasound | 51.4% (46.6%–56.1%) | 43.0% (38.0%–48.2%) | 57.9% (53.8%–61.9%) |
| Chest X-ray | 65.1% (60.5%–69.5%) | 59.4% (54.2%–64.4%) | 71.1% (67.3%–74.8%) |
| Additional microbiological sampling§ | 85.4% (81.7%–88.5%) | 85.8% (81.9%–89.2%) | 90.7% (88.0%–92.9%) |
| Source control | |||
| Initiation of rapid source control (surgical or interventional) | 57.4% (52.7%–62.1%) | 62.8% (57.7%–67.7%) | 70.6% (66.8%–74.3%) |
| Source control within 1–6 h | 33.8% (29.4%–38.4%) | 29.9% (25.3%–34.9%) | 40.2% (36.3%–44.3%) |
| Source control within 12 h | 12.2% (9.3%–15.6%) | 15.5% (12.0%–19.6%) | 15.6% (12.8%–18.8%) |
| Source control within 24 h | 2.5% (1.2%–4.4%) | 4.8% (2.9%–7.5%) | 3.9% (2.5%–5.8%) |
| No time frame | 1.6% (0.6%–3.2%) | 2.7% (1.3%–4.9%) | 2.0% (1.1%–3.5%) |
| Not specified | 7.4% (5.2%–10.3%) | 9.9% (7.1%–13.4%) | 8.8% (6.7%–11.4%) |
| Monitoring | |||
| Central venous catheter | 33.1% (28.7%–37.7%) | 36.9% (32.0%–42.0%) | 78.4% (74.9%–81.7%) |
| ScvO2 | 24.8% (20.8%–29.1%) | 27.5% (23.1%–32.4%) | 53.1% (49.0%–57.2%) |
| Arterial catheter | 30.2% (25.9%–34.7%) | 28.3% (23.8%–33.2%) | 74.9% (71.2%–78.3%) |
| Passive leg raising or fluid challenge | 48.2% (43.5%–53.0%) | 47.1% (41.9%–52.3%) | 65.5% (61.5%–69.4%) |
| Hemodynamic measurement‖ | 28.2% (24.0%–32.6%) | 33.2% (28.4%–38.2%) | 55.5% (51.4%–59.6%) |
| Antibiotic stewardship | |||
| Regular consultations with infectious diseases specialists | 29.7% (25.5%–34.2%) | 40.1% (35.1%–45.3%) | 39.6% (35.6%–43.6%) |
| Procalcitonin guided antiinfective therapy | 47.7% (43.0%–52.5%) | 52.7% (47.5%–57.8%) | 72.7% (68.9%–76.2%) |
| MRSA testing | 19.4% (15.8%–23.4%) | 26.5% (22.1%–31.3%) | 36.7% (32.8%–40.7%) |
Definition of abbreviations: MAP = mean arterial pressure; MRSA = methicillin-resistant Staphylococcus aureus; ScvO2 = central venous O2 saturation; SOFA = Sequential Organ Failure Assessment.
Data in parentheses are 95% CIs.
Begin rapid administration of 30 ml/kg of crystalloid for hypotension or lactate level ⩾4 mmol/L.
Apply vasopressors if patient is hypotensive during or after fluid resuscitation to maintain MAP ⩾65 mm Hg.
By clinical chemistry: white blood cells, coagulation, renal and liver function.
Examples: urine, swabs, cerebrospinal fluid.
Cardiac output, stroke volume, pulse pressure measurement.
QIIs and Sepsis Programs
A total of 31.4% of respondents (95% CI, 28.3%–34.7%) had programs available to increase the quality of sepsis care. QIIs across the whole hospital (ED, wards, and ICUs) existed on a regular basis in only 9.8% (95% CI, 7.9%–12.0%) of hospitals, with significant differences between the regions (P < 0.001) (Figure 4 and Table E18). Hospitals with QIIs had greater implementation of sepsis screening and standardized sepsis management in EDs, wards, and ICUs. Implementation of antibiotic stewardship and antimicrobial guidelines for patients with sepsis were also more common (Figure 5). According to the respondents, only 4.6% (95% CI, 3.3%–6.1%) of hospitals invested extra money in sepsis programs (Figure 4 and Table E25). Physicians and nurses from ICUs were more often part of the programs than staff from the ED or wards (Figure E21). Sepsis prevalence and mortality were monitored in 54.3% (95% CI, 51.0%–57.5%) and 45.0% (95% CI, 41.7%–48.2%) of all participating hospitals. Sepsis bundle compliance was measured in 18.1% (95% CI, 15.7%–20.7%) of hospitals, time to antibiotic therapy in 21.1% (95% CI, 18.5%–23.9%), severity of sepsis cases in 25.0% (95% CI, 22.3%–28.0%) and frequency of blood culture ordering in 47.5% (95% CI, 44.2%–50.7%).
Figure 4.
Quality improvement initiatives for sepsis in hospitals (n = 859).
Figure 5.
Implementation of screening and standardized management, antibiotic stewardship, and antimicrobial guidelines in hospitals with and without QIIs. The spider chart presents implementation of measures as proportions (percentages). ED = emergency department; QII = quality improvement initiative.
Infrastructure for Identification of the Source of Infection and Source Control
Imaging for Identification of the Source and Microbiological Diagnostic Service
Computed tomography or magnetic resonance imaging was available to identify the source of infection around the clock in 89.9% (95% CI, 87.8%–91.8%) of hospitals. The availability of an imaging service with computed tomography or magnetic resonance imaging with no time limitations was significantly higher in larger hospitals (Table E22). The microbiological diagnostic service was limited in time in 89.6% (95% CI, 87.6%–91.4%) of the hospitals. The limitations concerned a lack of the possibility to incubate blood cultures, identify pathogens, and communicate results outside the main working hours or during weekends and holidays. Services that were unlimited in time, including blood culture incubation, pathogen identification, and communication of results, were reported by only 106 of 1,023 (10.4%) hospitals.
Surgical and Interventional Source Control
Surgical service for source control that was unlimited in time was available in 87.0% (95% CI, 84.8%–89.0%) of the hospitals. The availability was highest in hospitals in Western Europe (95.5%; 95% CI, 92.7%–97.5%) and lowest in hospitals in Asia, Central and South America, and Africa (71.1%; 95% CI, 64.1%–77.5%). In hospitals with 0–250 beds, the availability was lower (79.9%; 95% CI, 74.9%–84.4%) than in hospitals with more than 250 beds (range, 88.9%–91.1%). There were no differences between general, university, and private hospitals (Table E23). The proportion of hospitals with services for interventional source control (e.g., by radiologists) that was unlimited in time was 31.7% (95% CI, 28.9%–34.7%). A small proportion of hospitals (5.3%; 95% CI, 4.0%–6.8%) had no services for source control available, leading to patient transfers.
Specific Measures for Hemodynamic Resuscitation and Antiinfective Treatment
Fluids, Hemodynamic Evaluation, and Management
Participants from hospitals with and without standardized sepsis management reported that balanced crystalloids were used more commonly than 0.9% NaCl in their ICUs for patients with sepsis (89.0% [95% CI, 86.7%–90.9%] vs. 39.7% [95% CI, 36.5%–43.0%]). Albumin was used by 40.8% (95% CI, 37.6%–44.1%) of respondents. Gelatin (8.0%; 95% CI, 6.3%–10.0%), hydroxyethyl starch (2.8%; 95% CI, 1.8%–4.1%), and dextran (1.7%; 95% CI, 0.9%–2.7%) were still used in some hospitals. There were significant differences in the use of fluids between regions (Figure E24). Norepinephrine (93.1%; 95% CI, 91.2%–94.6%) was by far the most common first-line vasoactive agent in ICUs (see Table E25).
Blood pressure and heart rate response (92.5%; 95% CI, 90.6%–94.2%) and urine output (92.2%; 95% CI, 90.2%–93.9%) were the most common parameters guiding fluid resuscitation in ICUs. Lactate clearance was used by 79.3% (95% CI, 76.5%–81.9%) of respondents as a measure to guide fluid resuscitation. Passive leg raising or fluid challenges were used for guidance more frequently than hemodynamic measurements like cardiac output, stroke volume, or pulse pressure variation (Table E26). Point-of-care lactate testing was available in 83.0% (95% CI, 80.2%–85.4%) of EDs, 44.8% (95% CI, 41.5%–48.1%) of wards, and 91.5% (95% CI, 89.5%–93.3%) of ICUs. It was more commonly available in EDs and ICUs in Northern and Western Europe than in other regions, but there were no significant differences between hospitals of different sizes or general and university hospitals (Table E27).
Antimicrobial Guidelines and Antibiotic Stewardship
The use of standard operating procedures or hospital guidelines for antimicrobial therapy for patients with sepsis was reported by 74.0% (95% CI, 71.1%–76.7%) of hospital representatives. The rate was higher in Northern Europe (92.8%; 95% CI, 85.7%–97.0%) and Western Europe (89.2%; 95% CI, 85.4%–92.3%) and lower in other regions: Southern Europe (63.9%; 95% CI, 56.4%–70.9%); Asia, Central and South America, and Africa (62.2%; 95% CI, 54.7%–69.3%); and Eastern Europe (59.6%; 95% CI, 52.6%–66.3%). There were no significant differences between hospitals of different sizes or types (Table E28). Antibiotic stewardship teams were most often implemented in Western Europe (80.4%; 95% CI, 75.7%–84.5%) and Northern Europe (77.4%; 95% CI, 67.6%–85.4%). In the wards, patients with sepsis were usually treated by the ward clinical teams (89.6%; 95% CI, 87.5%–91.4%), but 24.5% (95% CI, 21.8%–27.3%) of respondents stated that the treatment was regularly supported by infectious diseases specialists, and 18.1% (95% CI, 15.8%–20.7%) of participants indicated regular support by antibiotic stewardship teams (Table E29). Respondents stated that advice on antimicrobial treatment was available to ward clinicians in 83.3% (95% CI, 80.7%–85.7%) of hospitals and 84.3% (95% CI, 81.7%–86.7%) of ICUs (Table E30). To guide antiinfective management, procalcitonin was used widely in ICUs (72.7%; 95% CI, 68.9%–76.2%) and less frequently in wards (52.7%; 95% CI, 47.5%–57.8%) (Table 2).
Discussion
The results of this survey provide insight into sepsis care in 1,023 hospitals in 69 countries. Hospitals in the European Union included in the survey had a total of 388,000 acute-care beds, which corresponds to 23% of all acute-care beds in the European Union. Outside of Europe, only a limited number of hospitals were included in the study. Results suggest that, at a European level, we are a distance away from what the “golden goal” for a deadly disease should be.
Screening for sepsis has been recommended in international guidelines for more than 10 years (22, 23). In fact, the current international sepsis guidelines highlight screening for sepsis and the use of standard operating procedures for the management of sepsis as recommendation number one (2). Nevertheless, respondents stated that sepsis screening was implemented in only 62% of ICUs overall and even less often in EDs (54%) and wards (48%). In addition, screening was often not undertaken daily or available only on demand, resulting in potentially missed cases of sepsis. In contrast, hospitals with QIIs reached sepsis screening levels of >70%. The pattern for standardized sepsis management was similar, with substantially higher rates of standardized management in hospitals with QIIs. Implementation of antibiotic stewardship and hospital guidelines for antimicrobial therapy were also significantly higher in hospitals with QIIs (Figure 5). However, only 31.4% of hospitals had any QIIs, and few hospitals (9.8%) had implemented a regular QII across the whole hospital. The rate was lowest in Western Europe (5% for regular trainings), and university hospitals were not performing better than general hospitals.
A recent report of data from the National Healthcare Safety Network in the United States revealed that <10% of U.S. hospitals lacked a standardized screening process. Furthermore, >70% of U.S. hospitals had established guidelines or care pathways for the management of sepsis, and sepsis programs were reported in 73% of U.S. hospitals (24, 25).
In light of our findings and the data from the United States, we propose that participation in QIIs and sepsis programs should be regarded as best practice for achieving the World Health Organization recommendations (26), the Surviving Sepsis campaign guidelines (2), or national recommendations such as the National Institute for Health and Care Excellence guidelines (27) in the United Kingdom. Beneficial effects of QIIs were demonstrated in numerous studies (28–35), and there are also studies showing that such initiatives can be cost effective (32, 36–38). The U.S. Hospital Sepsis Program (39, 40) suggested seven core elements, including actions for identification and management but also for tracking outcomes and reporting. In our study, only 54% of respondents confirmed that sepsis prevalence was monitored and 45% stated that sepsis mortality was recorded. Also, the core element of “hospital leadership commitment” that demands the provision of necessary financial resources was hardly fulfilled. Respondents in our study indicated that financial support for sepsis programs was very low in their respective hospitals, with only 4.6% of hospitals investing in sepsis programs. The findings in our study are in stark contrast to those from the United States, where executive sponsors were reported by 55% of hospitals and sepsis was identified as a priority and communicated to staff in 72% of hospitals (24, 25).
Radiological imaging and general surgery are included in the standard infrastructure of hospitals, but their availability is also essential to identify the source of infection in a timely fashion and provide early source control (41–44). Furthermore, imaging and surgical and/or interventional source control are guideline recommendations (2, 26, 27, 45). In our study, imaging and surgical services were time-limited, especially in small hospitals (i.e., fewer than 250 beds). In addition, source control was often not an goal within the first 6 hours after the recognition of sepsis, necessitating patient transfer in some cases. These limitations may delay care and increase the risk of mortality (46). Another area of concern was the lack of microbiological diagnostics available on a 24-hour basis. In 90% of hospitals, blood culture diagnostics, which represent a critical component of sepsis treatment, was not accessible outside regular working hours. This can result in delays in the identification of pathogens, which in turn may impede the adaptation and optimization of antiinfective therapy. Negative consequences can include unnecessary or inadequate treatment, unnecessary selection pressure, and development of antimicrobial resistance and antimicrobial harm (47).
Based on these results, increased efforts are needed to improve sepsis care in hospitals, including: 1) amplified implementation of tools for the early identification of sepsis and 2) implementation of local treatment protocols based on international guidelines and local ecology and availability of resources.
Limitations
This survey has some limitations that need to be considered when interpreting the results. Most respondents and responses were from European hospitals, and only a very small number were from Asia, Africa, and Central and South America. Information from hospitals outside these regions was not collected. Therefore, the results reflect the situation in Europe. The study represents a convenience sample because participants contributed on a voluntary basis and may not have been representative. A potential selection bias cannot be excluded. A Hawthorne effect might have also influenced the results, whereby individuals modify an aspect of their behavior in response to being observed. It is independent of whether participants are selected randomly or nonrandomly (48). With every survey, the responses may be more positive or negative than in reality. However, it is likely that many of the hospitals where respondents worked have at least a basic interest in sepsis and quality of care. Given that >90% of respondents were hospital directors, heads of departments, or consultants, it can be assumed that they had a comprehensive understanding of the processes within their respective hospitals. However, it is important to acknowledge the inherent limitations of not conducting audits to validate the responses. In large hospitals, there may be significant discrepancies between different wards and departments. The intention of this study was to be exploratory, and generalization would not be appropriate. The results can only give an impression of the status in the 1,023 sampled hospitals. Finally, we acknowledge that we did not investigate adherence or compliance with existing screening programs.
Conclusions
The present study offers insights into sepsis care in hospitals across diverse geographical regions but mainly in Europe. The findings suggest that there is considerable room for improvement, particularly in a large number of European hospitals. This is especially true with regard to the early identification and standardized management of sepsis, the availability of guidelines, existence of diagnostic and therapeutic infrastructure, and the implementation of QIIs. These results underscore the necessity for more robust and comprehensive strategies to establish and implement comprehensive measures for sepsis identification, diagnostics, and evidence-based treatment, with the aim of establishing uniform quality standards.
Supplemental Materials
Acknowledgments
Acknowledgments
The authors thank the scientific boards/committees from the European Society of Intensive Care Medicine, European Society of Anaesthesiology and Intensive Care, European Society for Emergency Medicine, European Society of Clinical Microbiology and Infectious Diseases Study Group for Bloodstream Infections, Endocarditis and Sepsis, and Intensive Care Society United Kingdom, who reviewed the study protocol and questionnaire; the endorsing scientific societies, the European Society of Anaesthesiology and Intensive Care, European Society of Clinical Microbiology and Infectious Diseases Study Group for Bloodstream Infections, Endocarditis and Sepsis (from the European Society of Clinical Microbiology and Infectious Diseases), European Society for Emergency Medicine, European Society of Intensive Care Medicine, European Society of Paediatric and Neonatal Intensive Care, European Shock Society, Intensive Care Society United Kingdom, and International Fluid Academy, which supported the dissemination of the survey; all participants, including those who did not consent to being named in the collaborators list; and Simone Mancini from the Global Sepsis Alliance for organizing and coordinating the steering committee meetings.
Members of the European Sepsis Care Study Group are as follows: Wafaa Abdel-Elsalam, Alaa Abed, Fillip Abedinov, Marina Abramyan, Katie Adams, Jan Egil Afset, Mariia Agibalova, Murat Aipeissov, Halis Akalın, Firdevs Aksoy, Zainab Al Duhailib, Abdulrahman Al-Fares, Aiman Al-Touny, Shimaa Al-Touny, Adrià Albis, Tatjana Aleksic, Aslı Alkan, Sevil Alkan, Ghalib Almekhlafi, Almudena Alonso-Ojembarrena, Mustafa Alrabayah, Ahmed Subhy Alsheikhly, Jelmer Alsma, Hisham Althobaiti, Sabri Engin Altıntop, Simge Altuntaş, Particia Alvarez, Rute Alves, Ali Amanati, Lisa Amir, Fatma Ammari, David Andaluz Ojeda, Maria Andersson, Ana Andrijević, Stefan Angermair, Mariana Anghele, Goffredo Angioni, Sian Annakin, Djillali Annane, Bartosz Anuszkiewicz, Elżbieta Arłukowicz, Fernando Arméstar, Abel Arroyo, Sumalatha Arunachala, Abdullah Tarik Aslan, Theodoros Aslanidis, Ojan Assadian, Dorette Assen, Hakan Korkut Atalan, Sefika Nur Ayar, Gulbin Aygencel, Afzal Azim, Ahmad Azma Haryaty, Wannes Baeten, Vladimir Bagin, Iulia-Cristina Bagiu, Mirza Aun Muhammad Baig, Uliana Balan-Ilevskaia, Ruslan Baltaga, Herbert Baquerizo Vargas, Marco Barchetti, Anna Barcz, Vladislav Bardakhchyan, Lukas Barnas, Monica Baroni, Nelson Barros, Jesus Emilio Barrueco-Francioni, Joanna Bartczak, Michelangelo Bartolo, Onur Bas, Hulya Basar, Nicolae Batir, Jan-Hinrich Baumert, Oliver Beck, Marc Beckers, Mary Bedding, Ovidiu Horea Bedreag, Martin Beiderlinden, Albertus Beishuizen, Matija Belavić, Naya Bellaubí-Pallarés, Vladislav Belskii, Stepani Bendel, Jan Beneš, Patrik Benjaminsson Nyberg, Johan Berkius, Jana Berkova, Florian Berteau, Alessio Berttini, Samia Betout, Martin Bier, Mihaela Blaj, Sabine Blaschke-Steinbrecher, Ana Blázquez Abellán, John Bleasdale, Alexandre Bleibtreu, Auta Blessing, Dimitris Bliamplias, Constantine Bloch-Infanger, Florin Bobirca, Aleksandr Bobyshkin, Constantin Bodolea, Felix Boenhof, Pavel Boldyrev, Luigi Bonavina, Michael Booke, Gabriella Bottari, Yvonnick Boué, Hjalmar Bouma, Sebastian Brandt, Gennady Bregman, Violeta Briciu, Violeta Tincuta BriciuGiuseppe Brisinda, Nora Bruns, Nikola Brzanov, Serban-Ion Bubenek, Sonje Marina Bubonja, Ekaterina Budankova, Arnoldus Buenen, Michael Buerke, Dabota Buowari, Sara Cajander, Plinio Calligaro, Andrew Campbell, Can Aktaş, Ilkin Cankayalı, Zhanna Cansu, María Luisa Cantón Bulnes, Iacopo Cappellini, Valeria Caramello, Silva Carbajo Azabal, Nieves Carbonell, Antonio Carneiro, Andrea Carsetti, Reinoud Cartuyvels, Sulamita Carvalho-Brugger, Jan Castan, Miguel Castelo-Branco Sousa, Pedro Castro, Adriana Cataldo, Fausto Catena, Lucia Cattin, Martina Čehulić Širac, Martin Čermák, Christos Chaintoutis, Nilanchal Chakraborty, Agata Chalasiewicz, Athanasios Chalkias, Elena Chircov, Candan Cicek, José Pedro Cidade, Tatiana Ciomartan, Osman Sezer Cirit, Berta Cisteró Roig, Cristian Cobilinschi, Elif Colak, Cathal Collins, Anna Conen, Guglielmo Consales, Jorge Alejandro Contreras Jaquez, Brandusa Copacianu, Lupe del Rocio Coronel Chumbi, Ana Correia, Miguel Cortez, Augusto Cesar Costa Ferreira, Johan Courjon, Ben Creagh-Brown, Olaf L. Cremer, Aniek Crombach, Sofia Cuevas-Asturias, Martina Čurdová, Renata Curić Radivojević, Marko Cvetković, Piotr Czempik, Fabrizio D’Acapito, Stephanie D’Incau, Iita Daavittila, Michael Dalager-Pedersen, Dario Marietti, Swarup Das, Abhilash Dash, Mitesh Davda, Massimo De Cal, Bas De Groot, Maria De Marco, Silvia De Rosa, Nicolas De Schryver, Belinda De Simone, Vesna Degoricija, Mikhail Degtyar, Wissem Dehria, Douwe Dekker, Christopher Delaney, Türker Demirtakan, Secil Deniz, Dominique Descamps, Kevin Dewit, Ken Dewitte, Vipin Dhama, Ida Di Giacinto, Emilio Diaz, Juan Jose Diaz Diaz, Evgeni Dimitrov, Emine Kübra Dindar, Dan Sebastian Dîrzu, Michael Dolch, Raymond Dominic Savio, Laure Domisse, Katia Donadello, Laura Dono, Tom Dormans, Pavel Dostal, Sambhu Dutta, Jiri Dvorsky, Katarzyna Dzierzanowska-Fangrat, Anna Efthymiou, Anastasiya Egorova, Brigitta Ehrnström, Dominik Einwag, Anna Eklund, Andreas Ekman, Hakan Ekvall, Samia El Azab, Mohamed Elbahnasawy, Hussam Elqurashi, Hossam Elshekhali, Moataz Maher Emara, Luis Enseñat, Kanat Erbolat, Gul Erdem, Esma Eryilmaz-Eren, Esther Oviedo del Aguila, Selin Eyüpoğlu, Francisco Jose Ezponda Inchauspe, Beka Ezugbaia, Sami Fahoum, Pio Faust, Sergay Fedorov, Betânia Ferreira, Ricard Ferrer, Valeria Fico, Jan Fiersen, Pierre Fillatre, Mathias Fischer, Francesco Fleres, Mirela Flonta, Simin Aysel Florescu, Francois Fontana, Lorena Forcelledo, Maria Fortofoiu, Carmen Rosa Fraga Quintana, Irving Santiago Fraire Felix, Alessia Franceschi, Antonella Frattari, Christian Frey, Tina Frolo, Christina Füller, Rafal Galuszka, Lorenzo Gamberini, Joao Gamito Lopes, Julio César Garcia Casallas, Pablo García-Olivares, Roxana Garcia-Salcido, Piyush Garg, Aleksandra Gavrilovska-Brzanov, GC. Campello, Caterina Gentili, Ivanka Gergova, Michele Giannini, Patrik Gille-Johnson, Yves Gillet, Guy Glover, Sanja Golubic, Paulo Gomes, Gabriel Petre Gorecki, Vadim Gorokhovskiy, Udo Gottschaldt, Egor Govoruha, Dominic Grande, Serge Grazioli, Ioana Grigoras, Evgeny Grigoryev, Guillaume Grillet, Ioana Marina Grintescu, Alexey Gritsan, Heinrich Volker Groesdonk, Fredrik Grovan, Matjaž Groznik, Matthias Gründling, Caroline Grupp, Mario Guarino, Joern-Tryggve Guenther, Bertrand Guidet, Teresa Guimaraes, Nádia Guimarães, Raphael Gukasjan, Amit Gupta, Bikram Gupta, Manish Gupta, Gupta Ajay Kumar, Mohan Gurjar, Seda Guzeldag, Marton Gyenge, Michael Habenicht, Oliver Habler, Najah Hadi, Sebastian Hafner, Thomas Hahn, Raheela Hanif, Anamaria Harabor, Mohamed Hasaballah, Liudmila Hasak, Natasa Hasemaki, Mohamed Hassan, Nasser Hassan Abdalrady Hassan, Johanna Hästbacka, Andreas Hecker, Martin Helán, Frank Hendrich, Lucia Herbel, Juan Carlos Heredia Cedeño, María Juliana Hernández-Benito, Ivan Herold, Juan Antonio Hidalgo Ramos, Manfred Hoefler, Nihat Müjdat Hokenek, Aleksander Rygh Holten, Michal Holub, Claudia Holzbauer, David Honan, Cristina Honorato-Cia, Jacobien Hoogerwerf, Carla Hopper, Juan Horcajada, Petr Hubacek, Willemijn Barbara Huiszoon-Brummelhuis, Shihan Mahmud Huq, Pınar Hüseyin Ulaş, Miguel Ibarra-Estrada, Mercedes Ibarz Villamayor, Bushra Ibrahim-Baker, Miroslawa Idzik, Fatih Ileri, Bugra İlhan, Rosanda Ilic, Garba Iliyasu, Aikaterini Ioakeimidou, Orestis Ioannidis, Ionas Simutis, Daniela Ionescu, Ahtesham Iqbal, Anna Irga-Staniukiewicz, Arda Isik, Nahema Issa, Toni Ivičić, Artem Ivkin, Anshul Jain, Ville Jalkanen, Jarosław Janc, Slobodan Janković, Henry Jansen, Hilde Jansens, Susann J. Järhult, Björn Jäschke, Singh Jasvant, Yash Javeri, Etienne Javouhey, Pragnya Jena, Kim Jie, Shabbar Joad, Anna Jones, Silje Bakken Jørgensen, Romain Jouffroy, Marija Jovanovski-Srceva, Kazimir Juricic, Matija Jurjević, Karin Kaasjager, Maheen Kabir, Ebru Kacmaz, Vasileios Kaldis, Dominik Kallias, Madhusudan Kalluraya, Mrinal Kamal, Funda Karbek Akarca, Ildar Karimov, Eleni Karlafti, Hesham Keryakos, Christian Keuneke, Mohd Saif Khan, Almir Khasanov, Ekaterina Khinovker, Sergey Khomiakov, Kihoon Kim, Sung Hyun Kim, Mikhail Kirov, Thomas Kiss, Behçet Kılıç, Kirien Kjossev, Iris Klaus, Olga Klementova, Heinrich Klingler, Gerd Klinkmann, Hans Knotzer, Vladimir Kochergin, Jaromir Koci, Karolína Kočí, Klaus Kogelmann, Julia Kolbusz, Elina Kolho, Aidos Konkayev, Iris Koper, Csaba Kopitkó, Nikolaos Koronakis, Oksana Korshunkova, Zdenek Kos, Judit Kovacs, Sergeja Kozar, Sebastian Krämer, Markus Kredel, Michael Kremer, Andriy Krystopchuk, Maxim Kucher, Pınar Küçükdemirci-Kaya, Vladimir Kulabukhov, Anil Kumar, Neeraj Kumar, Ramesh Kumar, Rajesh Kumar, Pavel Kupka, Eray Kurnaz, Tatjana Kurucin, Biljana Kuzmanovska, Marcos J. Lago, Tobias Lahmer, Jaafar Lakhssassi, Nikolas Lambiris, Jean-Philippe Lanoix, Romaric Larcher, Annmarie Lassen, Nathalie Layios, Igor Lazic, Konstantin Lebedinskii, Andrei Lekmanov, Andrey Lenkin, Jose Leon Gonzalez, Rafael León Lopez, Adam Leoniuk, Sergey Lepshin, David Lerouge, Leo Licari, Monica Licker, Børge Lillebo, Adam Linder, Par Lindgren, Johan Lindstrom, Kirill Lipp, Oskar Ljungquist, Lars Ljungström, Ferran Llopis, Cristina López Viloria, F. Xavier López-Altimiras, Rüdiger Lott, Richard Lowsby, Jarosław Luboński, Filippo Luciani, García de Guadiana-Romualdo Luis, Anita Lukic, Mihaela Lupse, Niti Luthra, Lydia Lydia, Mariola Maciaszek, Karel Maelegheer, Sami Mäenpää, Mohamed Magdy, Ata Mahmoodpoor, Marcelo Maia, Antti Mäkelä, Pavel Malina, Ravikrishna Mamidanna, Kishore Mangal, Simone Mancini, Corina-Cecilia Manole-Pălivan, Anna Månsson, Salvatore Marchese, Luisa Marchioni, Elisa Marchionni, Soudani Marghli, Roman Marisov, Mariusz Siemiński, Demetra Markopoulou, Alessio Maroccia, Alejandro Martin-Quiros, Modesto Martinez Pillado, Alfredo Martins, Mehdi Marzouk, Elora Matanović, Elijah Matuvo, Afanasy Matveev, Ekaterina Matveeva, Martin Mauch, Oktawia Mazanowska, Anna Teresa Mazzeo, Carmelo Mazzeo, Maurizio Mazzoni, Karim Mechergui, Dario Melani, Lisa Mellhammar, Ahmad Meraj, Anna Meuronen, Evangelia Michailidou, Stephanie Mifsud, Mariana Mihaila, Julio Mijangos-Mendez, Malgorzata Mikaszewska-Sokolewicz, Ruth Milheiro, Georgi Minkov, Shakti Bedanta MishraIoan Remus Mitre, Magdalena Miulescu, Skule Mo, Onnen Moerer, Pablo Monedero, Nicolas Mongardon, Elisabeth Montel, Eleni Moraitou, J.Miquel Morales, Malte Morisse, Diego Morocho Tutillo, Paula Mota, Ashraf Butt, Sudipta Mukherjee, Apollo Mulyanti, Ana Maria Munteanu, Tatiana Musaeva, Xavier Muschart, Tomasz Musiuk, Biserka Mustac-Hlebec, Ventsislav Mutafchiyski, Olena Mutuka, Simon Nadel, Prashant Nasa, Tijana Nastasovic, Lukasz Naumiuk, Elena Neporada, Christian Nickel, Alexander Nicko, Batir Nicolai, Jeppe Sylvest Angaard Nielsen, Axel Nierhaus, Ruud Nijman, Filippia Nikolaou, Carla Nisii, Vasileios Nolas, Kuido Nomm, Maxim Nosenko, Georgios Notas, Andreas Nowak, Sinead O’Neill, Dušanka Obradović, Simon Oelsner, Esther Olaleye, Alessandra Oliva, Rosa Oltra, Uğur Önal, Kresimir Oremus, Çiğdem Orhan, Daniele Orso, Ulrich Ortler, Michael Osthoff, Stefan Ostmeier, Alexey Ovezov, Nida Özcan, Osman Can Öztürk, Osman Özüdoğru, Catarina Pacheco, Jacob Packmohr, José-Artur Paiva, Carlo Pallotto, Ivana Antonella Paolucci, Raffaella Papa, Marius Papurica, Nitish Kumar Parmar, Jeremie Pasquier, Débora O. Passos Pinheiro, Pavla Paterova, Patricia Patricio, Mical Paul, Jadranka Pavičić Šarić, Martina Pavletic, Robert Pederson, Kurt Pelgrims, Juan Pedro Peñalver Sanchez, António Manuel Pereira de Figueiredo, Bohdana Pereviznyk, Jose Luis Pérez-Fernández, Stefan Persson, Paula Pestana, Christoph Peter, Alina Petrica, Sirak Petros, Matthias Pfersdorff, Barbara Philips, Dominik Pichler, Yaroslav Pidhirnyi, Juan Francisco Piedra Rubio, Andrzej Pihowicz, F Javier Pilar-Orive, Silvana Pilia, Eric Pinck, Paulo Pinheiro, Claudia Plachtzik, Christoph Plank, Ulrich Plog, Nina Polze, Franz Ponce, Mihai Popescu, Georgi Popivanov, Olga Poplavskaya, Dmitriy Popov, Pedro Póvoa, Florian Prätsch, Gabriel Preda, Andreas Prengel, Denis Protsenko, Montserrat Pujol Jover, Rosario Cristoforo Puleo, Anni Pulkkinen, Alexey Pyregov, Raihan Rabbani, Gabriele Racanelli, Petar Radnev, Monika Rajani, Lukasz Rak, Marija Rakonjac, Marta Ramos, Alexandra Ramshorn-Zimmer, Aleš Rára, Pedro Rascado Sedes, Haroon Rashid, Krzysztof Ratnicki, Sebastian Rehberg, Martin Reichert, Karl Reiter, M K Renuka, Marco Resta, Joao Miguel Ribeiro, Eduardo A. Ribeiro de Castro, Niccolo Riccardi, Elina Riihioja, Marco Ripa, Caroline Riske, Irina Ristescu, Alba Rivera, Jürgen Rödel, Fernando Rodríguez Fernández-Reverte, María Dolores Rodríguez Mulero, Jan Roesner, Carolina S Romero, Ulrich Ronellenfitsch, Katy Rose, Serena Rossi, Nikoletta Rovina, Ester Rovira Lázaro, Snezana Rsovac, Hendrik Rüddel, Juan Carlos Ruiz-Rodriguez, Heiner Ruschulte, Irina Ruslyakova, Stefan Russwurm, Laura Ryan, Armin Sablotzki, Shikha Sachan, Ajit Sadangi, Amir Saeed, Zrinka Safaric Oremus, Chinmoy Sahu, Ismael Said-Criado, Boris Sakakushev, Samir Sakka, Giuseppe Salamone, Nigel Salter, Darya Salygina, Samir Samal, Aleksandr Samorodov, Line Samuelsson, Dorel Sandesc, Dutta Sanskriti, Sai Saran, Ali Sarı, Benjamin Sasko, Angela Saviano, Eva Schaden, Fredrik Schiöler, Dimitrios Schizas, Christian Schlottke, Matthias Schmauß, Tom Schmitz, Philipp Schütz, Martin Schwandt, Markus Schwendinger, Chen-June Seak, Saloni Sehgal, Armin Seibel, Ronald Seidel, Florian Seidlitz, Joana Selada, Gjulshen Selim, Bilal Sengu, Evren Şentürk, Nicolas Serck, Erica Sermijn, Lena Serrander, Aslan Shabanov, Bhagyesh Shah, Vitrag Shah, Pralay Shankar Ghosh, Konstantin Shapovalov, Sanjay Sharma, Aditya Nath Shukla, Valery Shvetsov, Khalid Siddiqi, Tomasz Siegel, Martin Siegemund, Rafael Sierra, Martin Sigurdsson, Ali H Sik, Adriana Silva, Anabela Leonor Silva Bártolo, Nuno Silva, Koen Simons, Tudor Dan Simu, Martina Sinai, Ritu Singh, Sergey Sinkov, Michal Sitina, Tomasz Skalec, Katarzyna Skawińska, Antonia Skotsimara, Kitty Slieker, Maria Slöcker-Barrio, Jakub Smiechowicz, Dimitris Smyrniotis, Janusz Sokolowski, Torill Solvaer Rosvoll, Orsolya Solymos, Kapil Dev Soni, Shiv Lal Soni, Masa Soric, Jens Soukup, David Southern, Savino Spadaro, Martin Spångfors, Alessandra Maria SpinelliMathias Sprenger, Namita Srivastava, Stefan Staar, Pascal Stammet, Patricia Stassen, Göran Stenlund, Petr Stepanek, Marija Stevic, Sanne Steyaert, Kelly Straka, Ditte Gry Strange, Birgitt Straub, Yulia Strezh, Nina Sulen, Sri Sunarmiasih, Christina Fjesme Sundby, Jonas Sundén-Cullberg, Martin Sundqvist, Jesper Svefors, Viktor Švigelj, Eileen Sweeney, Syed Shahrul Naz Syed Shamsuddin, Tamas Szakmany, Janos Szederjesi, Hakan Taban, Annelies Tacx, Silva Tafaj, Ömer Taikın, Tomáš Tajč, Mariola Talalaj, Lokman Hekim Tanriverdi, Darko Tasić, Polychronis Tasioudis, Pierre Tattevin, Fatih Tekin, Recep Tekin, Staffan Tevell, Andreas R. Thierbach, Inge Thoelen, Mark Timmermans, Ekaterina Tkachenko, Łukasz Tkaczyk, Matti Tolonen, Ivan Tomasi, Dana Tomescu, Tina Tomić Mahečić, Ibolya Toth, Sebastian Tranca, Stefano Trapassi, Nikita Trembach, Josep Trenado Álvarez, Maksim Tribulev, Filip Triest, Shiv Shanker Tripathi, Vincenzo Francesco Tripodi, Liubov Tsentsiper, Zeynep Ture, Sebastian Tuyls, Jonas Tverring, Niraj Tyagi, Ryhan Uddin, Mustafa Uğuz, Thomas Uhlig, Roxana Oana Ungurean, Sascha Ussat, Sandra Usuga Perilla, Liana Valeanu, Alda Valença, Silvia Valentini, Juha Valli, Mika Valtonen, Ilse Van Cotthem, Bea Van den Poel, Monique Van der Lugt, Bruno Van Herendael, Lenneke Van Lelyveld-Haas, Tom Van Severen, Martijn Van Tellingen, Stefanie Vandervelden, Philippe Vanhove, Marina Varela-Duran, Viviane Veiga, Paula Vera-Artazcoz, Nikolaas Verbeke, Anil Verma, Thessa Verniest, Isabelle Verstreken, Jiri Vesely, Pablo Vidal, Jean-Louis Vincent, Antonella Viola, Simona Viola, Francesca Viscosi, Oleg Voennov, Thomas Volk, Carlo Alberto Volta, Rouven-Alexander von Holten, Magnus von Seth, Antonija Vrbanić Šutalo, Bram Vrijsen, Evangelos Vryonis, Natalija Vukovic, Martin Wagner, Stig Walravens, Petra Wegermann, Christine Weis, Ingeborg Welters, Benedikt Wiggli, Eveny Winklaar, Stefan P. Wirtz, Rafał Wójtowicz, Phunsup Wongsurakiat, Nuria Worner Tomasa, Roelie M. Wösten-van Asperen, Magdalena Wujtewicz, Zhaoyang Xing, Michael Yaroustovsky, Dincer Yildizdas, Yvonne Young, Igor Zabolotskikh, Ewa Zabul, Maria Zach, Aleksandra Załustowicz, Kyriakos Zaragkoulias, Barbara Zawiślak, Marisa Zenaide Ribeiro Gomes, Yoann Zerbib, Elena Zilbert, Wolfgang Zink, Frank Zoerner, Konstantin Zolotukhin, Joanna Zorska, Nadezhda Zubareva, and Mehrun Zuleika.
Footnotes
Supported by the European Sepsis Alliance and an educational grant from Becton Dickinson SA. Becton Dickinson SA was not involved in the study design or recruitment or in writing, reviewing, or submission of the manuscript. This article represents the views of the named authors only.
Author Contributions: C.S.S., K.R., R.F., E.A.I., and M. Gründling contributed to the conceptualization. C.S.S., D.F., A.L., R.F., A.A., S.L., M. Ostermann, M. Gründling, E.J.G.-B., E.A.I., and K.R. contributed to the study design and harmonized the questionnaire. D.F., A.L., E.A.I., A.T.A., M.G.Ş., K.L., J.S., M. Gründling, and M. Osterman translated and checked the survey. C.S.S., M.K., M.V., and K.D., analyzed the data and produced the figures and tables. C.S.S. wrote the first draft of the manuscript. C.S.S., E.J.G.-B., D.F., A.L., E.A.I., M. Osterman, J.H., K.R., M.L.N.G.M., M. Gründling, and R.F. revised the article. R.F., D.A., A.A., A.T.A., G.B., H.R.B., V.C., R.C.R., K.D., M.E., M. Gründling, M. Gurjar, J.H., K.L., J.M., M.L.N.G.M., G.M., M. Osterman, M. Osthoff, J.A.P., M.S., J.S., S.L., M.G.S., A. Lassen, N.V. and K.Z. contributed as national coordinators or representatives of scientific societies to survey dissemination, were responsible for hospital recruitment, and checked participants. All authors contributed to data interpretation, provided substantial feedback on the article, and approved the submitted version.
C.S.S., E.J.G.-B., A.L., A.A. and D.F. are representatives of the European Sepsis Alliance. E.J.G.-B. is a representative of the Europeans Shock Society. R.F. and M. Ostermann are representatives of the European Society of Intensive Care Medicine. C.S.S., E.J.G.-B., E.A.I., A.T.A., and M. Osthoff are representatives of the European Society of Clinical Microbiology and Infectious Diseases Study Group for Bloodstream Infections, Endocarditis and Sepsis. G.B. is a representative of the European Society of Paediatric and Neonatal Intensive Care. S.L. is a representative of the European Society for Emergency Medicine. M.L.N.G.M. is a representative of the International Fluid Academy. M. Ostermann is a representative of the Intensive Care Society United Kingdom. K.R. is a representative of the Global Sepsis Alliance. D.F. is a representative of the European Society of Anaesthesiology and Intensive Care.
Availability of data and materials: the data used for this analysis can be made available upon reasonable request for as long as 5 years. For further information, please contact the corresponding author.
A data supplement for this article is available via the Supplements tab at the top of the online article.
Originally Published in Press as DOI: 10.1164/rccm.202406-1167OC on January 9, 2025
Author disclosures are available with the text of this article at www.atsjournals.org.
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Wirtz, Rafał Wójtowicz, Phunsup Wongsurakiat, Nuria Worner Tomasa, Roelie M. Wösten-van Asperen, Magdalena Wujtewicz, Zhaoyang Xing, Michael Yaroustovsky, Dincer Yildizdas, Yvonne Young, Igor Zabolotskikh, Ewa Zabul, Maria Zach, Aleksandra Załustowicz, Kyriakos Zaragkoulias, Barbara Zawiślak, Marisa Zenaide Ribeiro Gomes, Yoann Zerbib, Elena Zilbert, Wolfgang Zink, Frank Zoerner, Konstantin Zolotukhin, Joanna Zorska, Nadezhda Zubareva, and Mehrun Zuleika
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