Abstract
Purpose
Intensive care unit (ICU) patients are particularly susceptible to developing pressure injuries. Epidemiologic data is however unavailable. We aimed to provide an international picture of the extent of pressure injuries and factors associated with ICU-acquired pressure injuries in adult ICU patients.
Methods
International 1-day point-prevalence study; follow-up for outcome assessment until hospital discharge (maximum 12 weeks). Factors associated with ICU-acquired pressure injury and hospital mortality were assessed by generalised linear mixed-effects regression analysis.
Results
Data from 13,254 patients in 1117 ICUs (90 countries) revealed 6747 pressure injuries; 3997 (59.2%) were ICU-acquired. Overall prevalence was 26.6% (95% confidence interval [CI] 25.9–27.3). ICU-acquired prevalence was 16.2% (95% CI 15.6–16.8). Sacrum (37%) and heels (19.5%) were most affected. Factors independently associated with ICU-acquired pressure injuries were older age, male sex, being underweight, emergency surgery, higher Simplified Acute Physiology Score II, Braden score < 19, ICU stay > 3 days, comorbidities (chronic obstructive pulmonary disease, immunodeficiency), organ support (renal replacement, mechanical ventilation on ICU admission), and being in a low or lower-middle income-economy. Gradually increasing associations with mortality were identified for increasing severity of pressure injury: stage I (odds ratio [OR] 1.5; 95% CI 1.2–1.8), stage II (OR 1.6; 95% CI 1.4–1.9), and stage III or worse (OR 2.8; 95% CI 2.3–3.3).
Conclusion
Pressure injuries are common in adult ICU patients. ICU-acquired pressure injuries are associated with mainly intrinsic factors and mortality. Optimal care standards, increased awareness, appropriate resource allocation, and further research into optimal prevention are pivotal to tackle this important patient safety threat.
Electronic supplementary material
The online version of this article (10.1007/s00134-020-06234-9) contains supplementary material, which is available to authorized users.
Keywords: Decubitus epidemiology, ICU, Pressure injury, Pressure ulcer, Outcome, Risk factors, Morbidity, Mortality
Take-home message
| Pressure injuries are common in adult ICU patients and ICU-acquired pressure injuries are associated with mainly intrinsic factors, and mortality. Increased clinical awareness, appropriate resource allocation, and further investigations into the pathophysiology of pressure injuries in critical illness and optimal prevention strategies for ICU patients are pivotal to tackle this important patient safety threat. |
Introduction
Pressure injuries are localised lesions to the skin and/or underlying tissues due to pressure or pressure combined with shear [1, 2]. Often occurring at bony prominences, they can develop anywhere on the body. Predisposing factors include limitations in activity/mobility, deficiencies in nutrition and skin moisture, inadequate perfusion, and the use of mechanical devices that exert pressure on the skin [3, 4]. Frequently incorrectly considered a specific problem of long-term residents, they may develop as quickly as between the first hour and 4–6 h after sustained loading [5]. An international classification categorises the injuries into stages I–IV, Unstageable, and Suspected Deep Tissue Injury according to the extent of the tissue damage (Online Resource_2) [1, 2].
Pressure injuries cause pain and disability, compromise the quality of life [6], and extend the length of hospital stay by an average of 5–8 days per pressure injury [7]. By increasing the need for care resources they are a major economic burden for healthcare systems worldwide [8–10]. In the United States, the incremental hospital cost per patient of treating hospital-acquired pressure injuries is estimated at about US$10,708 and might exceed US$26.8 billion at the national level [11].
Patients residing in the intensive care unit (ICU) are extremely prone to developing pressure injuries due to their inherent immobility, haemodynamic instability, poor tissue perfusion and oxygenation, and to a plethora of complexly interacting intrinsic and extrinsic risk factors [12–14]. Additionally, they are highly exposed to medical devices [15]. Finally, medical and technological advances have generated a substantial ICU population of geriatric patients and long-term residents whose risk of developing pressure injuries might even be higher [16–18].
Despite the severity of the problem and the considerable unfavourable impact of these lesions on patient outcomes, patient care, and health economics, research interest in pressure injuries in the ICU population has remained restricted.
As a result, clear insight into the global epidemiology of pressure injuries in ICUs is still lacking [19]. A recent systematic review and meta-analysis on their occurrence in adult ICU patients found 10 studies published between 2002 and mid-2017 reporting cumulative incidences, and 12 providing prevalence data only [20]. Moreover, the included studies’ outcomes showed large variability. Cumulative incidence ranged from 3 to 39.3%, prevalence from 11.5 to 32.7%. These large differences cannot currently be explained due to a lack of large study cohorts capable of dealing with the clinical heterogeneity that is typical for the ICU setting, and with variations in the availability of healthcare resources worldwide.
The objective of this study was to provide an up-to-date picture of the extent and factors associated with pressure injuries in a large, geographically diverse cohort of adult ICU patients. More specifically, we aimed to identify the overall and ICU-acquired prevalence according to geographic region and anatomical location; risk factors associated with ICU-acquired pressure injuries; and the association of pressure injuries with hospital mortality. We hypothesised that a number of the individual patient and ICU contextual factors will be associated with the development of pressure injuries in adult ICU patients.
Methods
A full description is in Online Resource_3.
Study design and subjects
The Decubitus in Intensive Care Units study (DecubICUs) was a worldwide prospective, observational, 1-day point-prevalence study of pressure injuries among adult ICU patients with 12-weeks follow for survival status and length of hospital stay. All patients ≥ 18 years in ICU from 0:00 to 23:59:59 h on the study day were eligible; there were no exclusion criteria. DecubICUs was registered at ClinicalTrials.gov (NCT03270345).
Ethical approval
Overall, approval by established national, regional or local ethics committees and/or institutional review boards was granted.
Data collection
Data were collected on 15 May 2018. Alternative dates were set for Nigeria, Brazil and Libya due to delayed ethics approval. Anonymous patient data were collected by case report form. They encompassed demographic and admission data, and physiological data pertaining to the study day, including the severity of disease assessment by the Simplified Acute Physiology Score II (SAPS II) [21]. Pressure injury occurrence was measured by direct observation according to the international staging definitions [1, 2]. Pressure injury risk was assessed by the Braden scale that combines 6 subscales: mobility, activity, sensory perception, skin moisture, nutritional state, and friction/shear, with lower scores reflecting higher risk [22]. Follow-up data gathered were survival status, and length of ICU and hospital stay until hospital discharge or at 12 weeks following the study day (7 August 2018). The study protocol, including case and center report forms, is in Online Resource_4 and at https://www.esicm.org/research/trials/trials-group-2/decubicus/.
To maximise uniformity in reporting, we developed a training module with self-test on pressure injury staging (Online Resource_5) [1, 2] that was validated for content by 3 experts and published on the study website prior to study initiation. Registered participants were repeatedly encouraged to familiarise themselves with the module before data collection.
Data management
Quality and integrity of the reported data were checked. Missing, extreme or implausible values were returned to the local data collectors for review. Where data remained questionable, the primary investigators (SOL and SIB) made a final adjudication about study inclusion in mutual agreement. Missing values mutually judged eligible for inclusion were imputed with median values or deduced from other variables reported. Remaining missings were omitted from the analyses.
Statistical analyses
Analyses were performed at the patient level. Overall pressure injury prevalence was calculated as the proportion of the sample with at least one pressure injury on the study day, ICU-acquired prevalence as the proportion with at least one pressure injury acquired in ICU on the study day. Prevalence is reported as numbers (n) and percentages with 95% confidence intervals (CI). Continuous data are summarised by a median with interquartile range (IQR), categorical data as n (%). Univariate analyses used Chi square, Mann–Whitney U, and Kruskal–Wallis tests, as appropriate. Survival analysis was performed by Kaplan–Meier procedure (log-rank test). Associations with ICU-acquired pressure injuries were examined by generalized linear mixed-effects regression analysis with logit link function and a random effect for country. All variables were included following an exploratory approach, irrespective of univariate analyses results. As analyses did not focus on a prediction but on the identification of associations, feature selection was not applied, particularly as the risk of overfitting was minimised given the limited number of covariates (n = 24 for pressure injury occurrence, n = 22 for hospital mortality) and the adequate dataset size (n = 13,254). Results are reported as odds ratios (OR) with 95% CIs.
Statistical analysis was performed using IBM SPSS 24.0 (IBM Corp., NY, US) and R statistical software 3.6.1 [23].
Results
Hospitals and patients
We recruited 1117 ICUs in 90 countries (6 continents). Most were mixed medical-surgical units (n = 729; 65.2%) and in university hospitals (n = 675; 60.4%). Median (IQR) hospital and ICU capacities were 600 (329–1035) and 13 (8–20) beds, respectively; 1005 (89.9%) data collectors had studied a training module on pressure injury staging, of which 920 (82.3%) the module developed for this project. Participation rates and ICU characteristics are in Online Resources_6 and 7, respectively.
Data from 13,254 patients were eligible for analysis. Their demographic characteristics are in Table 1, completeness of data in Online Resource_8.
Table 1.
Characteristics of included patients
| Characteristic | All patients (n = 13,254; 100%)a | No pressure injuries (n = 9728; 73.4%)a | Pressure injuries (n = 3526; 26.6%)a | ICU-acquired pressure injuries (n = 2145; 16.2%)a |
|---|---|---|---|---|
| Age, years (M, IQR) | 64 (51–74) | 63 (50–74) | 66 (54–75) | 65 (53–74) |
| Sex (male) | 8184 (61.8) | 5923 (60.9) | 2261 (64.1) | 1414 (65.9) |
| Body Mass Index classb | ||||
| Underweight (< 18.5) | 680 (5.1) | 446 (4.6) | 234 (6.6) | 134 (6.2) |
| Normal weight (18.5–24.9) | 5287 (39.9) | 3944 (40.5) | 1343 (38.1) | 759 (35.4) |
| Pre-obesity (25–29.9) | 4420 (33.3) | 3259 (33.5) | 1161 (32.9) | 733 (34.2) |
| Obesity class I (30–34.9) | 1713 (12.9) | 1259 (12.9) | 454 (12.9) | 305 (14.2) |
| Obesity class II (35–40) | 690 (5.2) | 501 (5.2) | 189 (5.4) | 129 (6) |
| Obesity class III (> 40) | 464 (3.5) | 319 (3.3) | 145 (4.1) | 85 (4) |
| Mechanical ventilation on ICU admission | 7369 (55.6) | 5000 (51.4) | 2369 (67.2) | 595 (27.8) |
| Type of admission | ||||
| Medical | 6501 (49) | 4499 (46.2) | 2002 (56.8) | 1114 (51.9) |
| Elective surgery | 29 (22.5) | 2521 (25.9) | 457 (13) | 288 (13.4) |
| Emergency surgery | 2609 (19.7) | 1866 (19.2) | 743 (21.1) | 522 (24.3) |
| Trauma and burns | 1066 (8.8) | 842 (8.7) | 324 (9.1) | 221 (10.3) |
| Comorbidities | ||||
| Acquired Immune Deficiency Syndrome | 56 (0.4) | 35 (0.4) | 21 (0.6) | 16 (0.7) |
| Chronic Obstructive Pulmonary Disease | 1663 (12.5) | 1058 (10.9) | 605 (17.2) | 368 (17.2) |
| Malignancy | 1509 (11.4) | 1093 (11.2) | 416 (11.8) | 246 (11.5) |
| Cancer, solid tumour | 1089 (8.2) | 812 (8.3) | 277 (7.9) | 167 (7.8) |
| Metastatic cancer | 378 (2.9) | 280 (2.9) | 98 (2.8) | 47 (2.2) |
| Haematologic cancer | 233 (1.8) | 147 (1.5) | 86 (2.4) | 55 (2.6) |
| Immunocompromised | 968 (7.3) | 633 (6.5) | 335 (9.5) | 206 (9.6) |
| Corticosteroid therapy | 449 (3.4) | 271 (2.8) | 178 (5) | 106 (4.9) |
| Immunosuppression | 444 (3.3) | 279 (2.9) | 165 (4.7) | 107 (5) |
| Chemotherapy | 313 (2.4) | 228 (2.3) | 85 (2.4) | 55 (2.6) |
| Cirrhosis | 433 (3.3) | 314 (3.2) | 119 (3.4) | 60 (2.8) |
| Diabetes | 2842 (21.4) | 1913 (19.7) | 929 (26.3) | 534 (24.9) |
| Heart failure | 1752 (13.2) | 1132 (11.6) | 620 (17.6) | 373 (17.4) |
| Impaired mobility | 1680 (12.7) | 1067 (11) | 613 (17.4) | 311 (14.5) |
| Malnutrition | 651 (4.9) | 359 (3.7) | 292 (8.3) | 138 (6.4) |
| Peripheral vascular disease | 662 (5) | 408 (4.2) | 254 (7.2) | 146 (6.8) |
| Renal failure | 1416 (10.7) | 898 (9.2) | 518 (14.7) | 320 (14.9) |
| Simplified Acute Physiology Score II categoryc | ||||
| ≤ 23 | 3473 (26.2) | 2985 (30.7) | 488 (13.8) | 304 (14.2) |
| 24–33 | 3335 (25.2) | 2616 (26.9) | 719 (20.4) | 431 (20.1) |
| 34–44 | 2955 (22.3) | 1973 (20.3) | 982 (27.9) | 595 (27.7) |
| ≥ 45 | 3491 (26.3) | 2154 (22.1) | 1337 (37.9) | 815 (38.0) |
| Braden score categoryd | ||||
| Very high risk (≤ 9) | 1448 (10.9) | 849 (8.8) | 599 (17) | 53 (2.5) |
| High risk (10–12) | 3928 (29.6) | 2491 (25.8) | 1437 (40.8) | 365 (17) |
| Moderate risk (13–14) | 2474 (18.8) | 1743 (18.1) | 731 (20.8) | 463 (21.6) |
| Mild risk (15–18) | 3689 (27.8) | 3039 (31.5) | 650 (18.5) | 878 (41) |
| No risk (19–23) | 1635 (12.3) | 1534 (15.9) | 101 (2.9) | 383 (17.9) |
| Length of stay in ICU prior to study day (M, IQR) | 4 (1–12) | 3 (1–9) | 10 (4–25) | 13 (5–29) |
| Length of stay in ICU (M, IQR) | 11 (4–28) | 8 (3–21) | 22 (10–46) | 27 (13–52) |
| Length of stay from ICU admission to hospital discharge (M, IQR) | 19 (9–40) | 16 (8–33) | 31 (15–57) | 36 (19–62) |
| Length of stay in hospital after study day (M, IQR) | 12 (6–27) | 10 (5–23) | 17 (7–35) | 19 (8–36) |
| Patients still in ICU 3 months after study day | 178 (1.3) | 129 (1.3) | 49 (1.4) | 30 (1.4) |
| Patients still in non-ICU ward 3 months after study day | 781 (5.9) | 531 (5.5) | 250 (7.1) | 171 (8) |
| Deceased during hospital stay | 2929 (22.1) | 1663 (17.1) | 1266 (35.9) | 812 (37.9) |
| 28-days mortality | 1751 (13.2) | 1149 (11.8) | 606 (17.2) | 340 (15.9) |
Results are expressed as number (percentages) if not differently indicated
ICU intensive care unit, M median, IQR interquartile range
aTotals may not sum to 13,254, 9728, 3526 and 2145, respectively, owing to missing values; an overview of the completeness of data is in Online Resource_8
bBody Mass Index is body weight in kilograms divided by body height in meters squared
cRange of possible scores is 0–163; a higher SAPS II score indicates a higher severity of disease and acute illness; scores are categorized according to the sample’s quartiles
dRange of possible scores is 6–23
Prevalence
We identified 6747 pressure injuries in 3526 patients, of which 3997 were ICU-acquired (59.2%; 2145 patients). Overall, 2081 patients had 1 pressure injury, 653 patients had 2, 411 had 3, and 381 had > 3 pressure injuries; and 1284 patients had 1, 398 had 2, 243 had 3, and 220 had > 3 ICU-acquired pressure injuries. Injuries were acquired before ICU admission in 1381 patients; developed in the ICU in 1922; and 233 patients developed injuries both before and during ICU stay.
Table 2 reports the overall and ICU-acquired prevalence across the 6 continents. A detailed breakdown per Stages and continents is in Online Resource_9. The overall prevalence was 26.6% (95% CI 25.9–27.3) with 18.0% (95% CI 17.3–18.6; n = 2383/13,254) of stage II or worse. Overall stage II prevalence was 11.4% (95% CI 10.9–11.9), stage III prevalence 4.2% (95% CI 3.9–4.6), and stage IV prevalence 2.0% (95% CI 1.7–2.2). Prevalence of Unstageable and Suspected Deep Tissue Injuries was 2.1% (95% CI 1.9–2.4) and 2.3% (95% CI 2.1–2.6), respectively.
Table 2.
Overall and ICU-acquired pressure injury prevalence according to continents
| All n = 13,254 |
Europe n = 5632 |
North America n = 1507 |
Latin, Central and South America n = 1040 |
Asia n = 4424 |
Africa n = 246 |
Oceania n = 405 |
|
|---|---|---|---|---|---|---|---|
|
Number of patients (percentage) 95% confidence interval |
|||||||
| Overall prevalence |
3526 (26.6) 25.9–27.3 |
1630 (28.9) 27.8–30.1 |
344 (22.8) 20.8–25 |
365 (35.1) 32.2–38.1 |
1047 (23.7) 22.4–25 |
84 (34.2) 28.5–40.1 |
56 (13.8) 10.8–17.5 |
| ICU-acquired prevalence |
2145 (16.2) 15.6–16.8 |
1124 (20) 18.9–21 |
200 (13.3) 11.7–15.1 |
237 (22.8) 20.3–25.4 |
495 (11.2) 10.3–12.2 |
52 (21.1) 16.5–26.7 |
37 (9.1) 6.7–12.3 |
| Proportion ICU-acquired prevalence (%) | 60.8 | 69.0 | 58.1 | 64.9 | 47.3 | 61.9 | 66.1 |
Results are expressed as number of patients (percentages) and 95% confidence interval if not differently indicated. Online Resource_9 reports more detailed information distributed for distinct pressure injury Stages
ICU intensive care unit
ICU-acquired prevalence was 16.2% (95% CI 15.6–16.8), with 11.0% (95% CI 10.5–11.5) of stage II or worse. ICU-acquired stage II prevalence was 7.5% (95% CI 7.1–8); stage III prevalence 3.2% (95% CI 2.9–3.5), and stage IV prevalence 1.7% (95% CI 1.5–1.9). ICU-acquired prevalence of Unstageable and Suspected Deep Tissue Injuries was 2% (95% CI 1.7–2.2) and 2% (95% CI 1.8–2.3), respectively.
ICUs from low and lower-middle-income economies, where the mean percentage of gross national income spent on healthcare is least, reported the highest overall prevalence of pressure injuries (40.7%, 95% CI 36.7–44.8) and of ICU-acquired pressure injuries (27.7%, 95% CI 24.1–31.5; Online Resource_10).
The sacral region and heels were the most affected anatomical sites, accounting for 37 and 19.5% of all pressure injuries, respectively. Figure 1 shows numbers (percentages) of overall and ICU-acquired pressure injuries at the most affected body locations. A comprehensive overview of all body locations according to pressure injury staging is in Online Resource_11.
Fig. 1.
Anatomical locations of pressure injuries (most affected body sites). Left: Numbers (percentages) of overall pressure injuries − total number of pressure injuries = 6764. Right: Numbers (percentages) of intensive care unit-acquired pressure injuries − total number of pressure injuries = 3997
Factors associated with ICU-acquired pressure injuries
Generalized linear mixed-effects regression analysis identified the following factors as independently associated with ICU-acquired pressure injuries: older age, male sex, being underweight, admission due to emergency surgery, decreasing Braden scores, increasing ICU stay, chronic obstructive pulmonary disease, immunodeficiency, renal replacement therapy, mechanical ventilation on ICU admission, higher SAPS II score, and being in a low or lower-middle-income economy, with strongest, gradually increasing associations with worsening Braden scores and increasing length of ICU stay before the study day, respectively (n = 12,533; Table 3).
Table 3.
Factors independently associated with ICU-acquired pressure injury
| Variable | Odds ratio | 95% confidence interval |
|---|---|---|
| Admission type: medical | 1.15 | 0.94–1.4 |
| Admission type: elective surgery | 1.02 | 0.8–1.29 |
| Admission type: emergency surgery | 1.28 | 1.04–1.58 |
| Age | 1.005 | 1.0007–1.009 |
| Male sex | 1.21 | 1.08–1.36 |
| Body Mass Index | ||
| 18.5–24.9: normal weight | Reference | |
| < 18–5: underweight | 1.58 | 1.23–2.01 |
| 25–29.9: pre-obesity | 1.03 | 0.9–1.17 |
| ≥ 30: obesity | 0.98 | 0.84–1.14 |
| Risk of pressure injury | ||
| Braden score 19–23: no risk | Reference | |
| Braden score 15–18: mild risk | 2.91 | 1.81–4.68 |
| Braden score 13–14: moderate risk | 5.23 | 3.25–8.42 |
| Braden score 10–12: high risk | 6.52 | 4.07–10.44 |
| Braden score ≤ 9: very high risk | 9.72 | 6.01–15.71 |
| Acquired immune deficiency syndrome | 1.52 | 0.74–3.11 |
| Cirrhosis | 0.89 | 0.65–1.22 |
| Chronic obstructive pulmonary disease | 1.24 | 1.03–1.49 |
| Diabetes | 1.05 | 0.92–1.2 |
| Heart failure | 1.07 | 0.92–1.25 |
| Immunocompromised | 1.27 | 1.04–1.55 |
| Malignancy | 0.95 | 0.8–1.14 |
| Peripheral vascular disease | 1.19 | 0.95–1.51 |
| Days in ICU before study day | ||
| 0–3 days | Reference | |
| 4–6 days in ICU before study day | 2.28 | 1.90–2.74 |
| 7–9 days in ICU before study day | 3.57 | 2.91–4.37 |
| 10–12 days in ICU before study day | 4.12 | 3.29–5.17 |
| > 12 days in ICU before study day | 7.51 | 6.42–8.78 |
| Mechanical ventilation on admission | 1.26 | 1.11–1.43 |
| Sedation | 0.95 | 0.82–1.09 |
| Muscle relaxant use | 1.08 | 0.83–1.41 |
| Vasopressor use | 1.04 | 0.91–1.2 |
| Renal replacement | 1.34 | 1.14–1.58 |
| Simplified Acute Physiology Score II score | 1.006 | 1.002–1.01 |
| Number of patients per nurse | 0.91 | 0.83–0.99 |
| Economya | ||
| High-income economy | Reference | |
| Upper-middle income economy | 1.09 | 0.65–1.85 |
| Low- + lower-middle income economy | 1.82 | 1–3.29 |
aEconomy: categorised according to the 2016 World Bank classification (https://data.worldbank.org/indicator/SH.XPD.CHEX.GD.ZS)
Hospital mortality
Overall hospital mortality was 22.5% (95% CI 21.8–23.3; n = 2929/12 989). Following adjustment for demographics and morbidity data, severity of pressure injury showed a gradually increased association with hospital mortality: OR 1.31 (95% CI 1.1–1.55) for stage I, OR 1.66 (95% CI 1.41–1.95) for stage II, and OR 2.31 (95% CI 1.96–2.71) for stage III or worse, i.e. stage IV, Unstageable, or Suspected Deep Tissue Injury (n = 11 889; Online Resource_12). Figure 2 reports survival distribution for patients with increasing severity of pressure injuries (i.e., no pressure injury, stage I, stage II, and stage III or worse; Log-rank test: p < 0.001).
Fig. 2.
Kaplan–Meier estimates of overall survival according to pressure injury status on the study day among adult intensive care unit patients. Green line indicates patients without pressure injuries; yellow line indicates patients whose worst pressure injury is of stage I; orange line indicates patients whose worst pressure injury is stage II; red line indicates patients whose worst pressure injury is stage III or worse (i.e. stage IV or Unstageable or Suspected Deep Tissue Injury). Tick marks indicate censored data (hospital discharge before 12 weeks). Log-rank test: p < 0.001
Discussion
In this point-prevalence study encompassing 1117 ICUs in 90 countries across 6 continents and involving 13,254 adult patients, we found an overall pressure injury prevalence of 26.6% and an ICU-acquired prevalence of 16.2%. Although the prevalence was highest in low and lower-middle-income economies, our findings suggest that pressure injuries remain a considerable burden for healthcare systems worldwide, and highlight the necessity of additional efforts in patient safety initiatives.
These observational data confirm and reinforce previous findings resulting from meta-analysis [20]. Additionally, they are complementary to findings from systematic reviews aiming at determining risk factors for pressure injuries in ICU patients [12, 24–26]. These identified a broad range of factors including age, length of ICU stay, diabetes, mechanical ventilation, vasopressor support, hypotension, and cardiovascular disease, and suggest that an interplay of these factors increases the probability of pressure injury development. Our data, albeit resulting from cross-sectional research and thereby only representing the study day, are suggestive for associating pressure injury in ICU with a patient profile characterised by high vulnerability, as evidenced by the following findings. First, the occurrence of pressure injuries was associated with the Braden score, which summarises essential conditions that gradually contribute to a high-risk profile characterised by being bedridden, malnourished, incontinent, and with limited ability to react on or sense pain [22]. These conditions are characteristic for a majority of ICU patients and mirror an overall vulnerability level. Second, older age was independently associated with pressure injury occurrence. The steadily increasing proportion of very old ICU residents constitutes an overt influx of high-risk patients given the accumulation of chronic comorbidities, nutritional deficiencies, immobility, and aging skin [17, 18]. Third, an association was found with organ support (mechanical ventilation and renal replacement therapy), which implies a high severity of acute illness. Finally, this high-vulnerability profile is completed by the finding that patients who resided > 12 days in ICU before the study day had a 7.5-fold increased risk of ICU-acquired pressure injury compared to patients with a short ICU stay (≤ 3 days).
As such, our data suggest that the large majority of factors associated with pressure injury in ICU patients appear to be intrinsic or unmodifiable. This is in line with the unanimous agreement of experts that pressure injuries can be unavoidable in haemodynamically unstable or critically ill/injured individuals [27]. Our findings need validation, preferably in longitudinal studies. Prospective high-resolution data from smaller samples might also identify additional modifiable factors not sought in this study. A hint that these may exist is the lower prevalence reported in Asia where increased awareness may have been prompted by previous large-scale initiatives on this topic. Until such data is generated, the variables we identified can at least be used to flag patients who might benefit from greater vigilance for pressure injuries. Also research into pressure injury pathophysiology and prevention specifically directed towards the heterogeneous ICU population is recommended.
Another factor independently associated with pressure injury was being in a low or middle-low income economy ICU. Limited availability of human and material resources may contribute to this finding, as the mean percentage of gross national income spent on healthcare in these economies is less than half as compared with high-income economies (4.9% versus 10.3%). Additionally, pressure injury prevention might not be a healthcare priority in developing countries.
Manzano and co-workers [28] identified pressure injury as a significant independent predictor of mortality in mechanically ventilated patients (adjusted hazard ratio 1.28; 95% CI 1.003–1.65; p = 0.047). The mortality associated with pressure injuries remains however unclear. As their occurrence often mirrors a generally debilitated condition and high severity of acute illness, an association with mortality seems reasonable. However, our regression analysis demonstrated a gradual increase in mortality with increasing severity of pressure injuries despite adjustment for these covariates. Even though this does not imply causality, this observation calls for clinical concern towards patients presenting with pressure injuries or those at high-risk for developing such complications.
Stage I pressure injuries are generally considered reversible if promptly identified and appropriately managed [13] and, therefore, often excluded from scientific reports [19]. They were nevertheless shown to be prone to deterioration, as in 6 Dutch acute care hospitals where 22.1% worsened to a deeper lesion [29]. In line with several earlier prevalence reports [29], the majority of pressure injuries in our study were of stage I (38.1%). These currently often underreported injuries, however, emerged from our analyses as independently associated with hospital mortality, which calls for considering these lesions as full quality indicators and for the standardized recording of this data in institutional and research reports.
This study has limitations. The cross-sectional design might have resulted in bias toward patients who have long ICU stays [30]. Since the length of stay is associated with pressure injury risk, the reported prevalence might not be representative for the entire ICU population. Our data only represents a snapshot at the study day and cannot account for potentially influencing factors such as staffing levels. Data on pressure injuries on mucosal surfaces have not been collected as these are not staged by the international staging system [4]. Not all geographic regions are well-represented, thus impeding globally generalized results. As pressure injuries might be considered as a result of suboptimal care, fear of criticism or institutional censure may have hampered objective reporting. If so, the actual prevalence might be higher than the rates identified. Accurate assessment of pressure injury staging is challenging and data collectors were not required to be qualified tissue viability experts. Despite our efforts to obtain consistency in reporting using a well-documented data collection procedure and providing a training module, variability and errors in staging may have occurred. Given the scale of the study, it was however not feasible to assess the validity of the data using digital photographs. Nevertheless, the error resulting from our approach will if anything have led to random error in estimations, rather than a systematic error. We were unable to doublecheck the self-reported number of participants who indicated having studied the training module, which may be prone to social desirability bias. As we requested to report the number of ‘nurses’ on the study day, without further definition, we do not know whether assistant-nurses were also reported and included in the calculation of the number of patients-per-nurse. The unexpected association of this variable with pressure injury also needs further exploration. There is a view that Suspected Deep Tissue Injuries should not be included in epidemiological studies because it is unclear how many are actual deep tissue injuries that convert to pressure injuries. Their number was however small and unlikely to have substantial impact, if any, on the estimated prevalence. Finally, our study may be prone to random observer errors as data collectors depended on the reliability of patient files to determine whether a pressure injury was ICU-acquired.
The major strength is that it is the first to present a worldwide picture of the epidemiology of pressure injuries in adult ICU patients and to map a high-risk profile based on a large global sample. It may act as an incentive for tackling this patient safety issue and provide local and regional baseline data for quality improvement programmes. Furthermore, pressure injuries staging was assessed by the gold standard of skin inspection by trained outcome assessors, and the study used a rigorous protocol with clear attention to detail in standardising the data collection process.
Conclusions
This observational study identified a quarter of ICU patients with pressure injuries albeit with considerable regional variation in prevalence. However, approximately 60% of the patients developed these lesions in ICU irrespective of the regional prevalence. As pressure injuries are a common complication and a substantial burden for healthcare systems worldwide, their prevention deserves increased clinical awareness and appropriate resource allocation. Besides, further investigations into the pathophysiology of pressure injuries in critical illness and into optimal prevention strategies for ICU patients are pivotal to tackle this important patient safety threat.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Author contributions
SOL and SIB prepared the first draft. SOL, SIB and MD analysed the data. GF managed study registrations and the online platform for data collection. SJB, WC, AKK, and LS provided first internal reviewer feedback. All authors provided data, developed models, reviewed results, provided guidance on methods, and reviewed the manuscript. SOL, SIB and MD finalised the manuscript on the basis of comments from all authors. All authors approved the final version. SOL, SIB, and GF had full access to all the data in the study. SOL and SIB had final responsibility for the decision to submit for publication.
Funding
This project received funding from the European Society of Intensive Care Medicine (ESICM), the Flemish Society for Critical Care Nurses, and the HOGENT Fund for Applied Research. SB holds a research mandate from the Special Research Fund at Ghent University. In the UK, infrastructure support was provided by the National Institute for Health Research (NIHR) Imperial Biomedical Research Centre (BRC). The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health and Social Care. LR was funded by a TD Nursing Professorship in Critical Care Research from Sunnybrook Research Institute, Toronto, Canada. The ESICM financed and co-administered the online data collection platform, provided a study webpage, and supported study administration. The other funding sources had no role in this work.
Availability of data and material
Study protocol, statistical analysis plan, and informed consent forms will be shared upon request with any researcher. Local DecubICUs investigators have the right to use the data collected from their respective units. National data can be obtained and used by the DecubICUs National Representatives upon proof of written consent from the local investigators. The complete DecubICUs database is only transferred to the primary investigators, SOL and SIB. They cannot share the database as they are bound to a broad variety of Data User Agreements. Information requests are to be addressed to stijn.blot@ugent.be and sonia.labeau@hogent.be.
Compliance with ethical standards
Conflicts of interest
Received honoraria or grants outside the submitted work: Ashish K. Khanna (Medtronic, Philips North America, Edwards Lifesciences, Zoll Medical, La Jolla pharmaceuticals, and Retia Medical). Stijn I. Blot (Pfizer, 3M). Leif Saager (Medtronic, Merck, The 37 Company, Ferrer Deutschland). For the other authors, there are no conflicts of interest.
Code availability
Not applicable.
Footnotes
The original online version of this article was revised: the ESICM Trials Group Collaborators were not tagged correctly.
The complete list of the DecubICUs study Team and ESICM Trials Group study collaborators is in Online Resource_1.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Change history
2/26/2021
A Correction to this paper has been published: 10.1007/s00134-020-06327-5
Contributor Information
Stijn I. Blot, Email: stijn.blot@UGent.be
the European Society of Intensive Care Medicine (ESICM) Trials Group Collaborators:
Dritan Muzha, Antoni Margarit Ribas, Fernando Lipovesty, Cecilia Loudet, Fiona Coyer, Philipp Eller, Nafseen Mostafa, Patrick M. Honoré, Vanesa Mercado Telleria, Jasmina Smajic, Paula Cristina Nogueira, Khalid Mahmood Khan Nafees, Romuald Hentchoya, Louise Rose, Javiera Soledad, Frances Lin, Yenny Cardenas, Amylkar Garay Reyes, Alan Sustic, Meropi Mpouzika, Tamas Vymazal, Hanne Irene Jensen, Hernan Aguirre-Bermeo, Liivi Maddison, Maija Valta, Silvia Calvino-Gunther, Frank Bloos, Faustina Excel Adipa, Vasilios Koulouras, Judy Enamorado, Zsuzsann Ágoston, Hrönn Birgisdóttir, Amit Gupta, Mohan Gurjar, Bram Kilapong, Seyed Mohammadreza Hashemian, Ignacio Martin-Loeches, Julie Benbenishty, Andrea Cortegiani, Kelly Fletcher, Yoshiro Hayashi, Wangari Waweru-Siika, Khalid Abidi, Sang-Min Lee, Burhan Hadri, Mihails Dolgusevs, Fayez François Abillama, Tomas Jovaisa, Cyril Thix, Muhammed Elhadi, Basri Mat Nor, Shanti Ratnam, Mohd Zulfakar Mazlan, Sundaresan Maiyalagan, Luis Sánchez-Hurtado, Adrian Belii, Mendsaikhan Naranpurev, Prabha Gautam, Dylan De lange, Rachael Parke, Rose Ekama Ilesanmi, Mirjana Shosholcheva, Antonija Petosic, Ranveig Lind, Madiha Hashmi Ffarcsi, Javier Bogarin, Aaron Mark Hernandez, Malgorzata Mikaszewska-Sokolewicz, Bruno Sousa, Dana Tomescu, Dorel Sandesc, Theogene Twagirumugabe, Vitaly Gusarov, Maie Ebaid, Radmilo Jankovic, Gari Slobodianiuk, Andrea Martonova, Rihard Knafelj, Mervyn Mer, Emilio Maseda, Bernardo Panka, Joerg C. Schefold, Eva Joelsson-Alm, Konlawij Trongtrakul, Lorna Merritt-Charles, Lamia Ouanes Besbes, Yalım Dikmen, Lesia Zgrzheblovska, Mark Fielding, Francesca Rubulotta, Ashish K. Khanna, Leif Saager, Ingrid von der Osten, Dritan Muzha, Alban Greca, Alma Cani, Nordian Xhindi, Genci Hyska, Antonio Margarit Ribas, Susana Pinto, Paulo Alves, Romina Esposito, Emanuel Valgolio, John Thomas Sanchez Minope, Antonio Abdala, Maria Ayala, Silvina Bravo, Ana Bantar, Patricia Delgado, Gustavo Badariotti, Fernando Lipovestky, Ana Diaz, Pablo Saul, Mariano Setten, Alejandra Aucapina, Ysica Acosta, Victor Gonzalez, Luis Camputaro, Fernando Baccaro, Robert Villa, Ana Diaz, Marcela Mastantuono, Emiliano Dean, Oscar Fernández Rostello, Patricia Brizuela, Julio Ricardo Bartoli, Matias Guereschi, Cristian Quiroga, Sofia Putruele, Paula Villegas, Veronica Curilen, Ruben Fernandez, Mariangeles Gabriela Nocheretti, Rosana Gabriela Escalante, Cecilia Inés Loudet, Silvia Fernandez, Ana Laura Gonzalez, Gustavo Andres Alvarez, Federico Iglesias, Silvia Chaparro, Graciela Zakalik, Gonzalo Pagella, Matías Baini, Pierina Arias Campos, Ignacio Sabbag, Armando Schmukler, Imelda Perdomo Fonseca, Gonzalo Martín Alvarez, Mario Ramirez, Fernando Tapia, Carlos Alejandro Bascary, Graciela del Valle Gimenez, Fernando Pablo Bertoletti, Esteban Milioto, Pablo Julio Maldonaldo Bonsignore, Maria Alejandra Fernandez, Julie Smith, Tim Chimunda, Lorraine Thompson, Teena Maguire, Frances Lin, Wendy Chaboyer, Fiona Coyer, Stacey Watts, Marion Mitchell, Madeleine Powell, India Lye, Leanne Parsons, Nerilee Baker, Claire Reynolds, Amy Thompson, Kristy Masters, Kellie Sosnowski, Lynette Morrison, Gavin D. Leslie, Ramanathan Lakshmanan, Alexis Tabah, Wendy Brown, Sharon McDowell-Skaines, Andrea McLucas, Chris Smith, Mandy Tallot, Sarah Jones, Michelle Barakat-Johnson, Thomas Leong, Rand Butcher, Kerrie Martin, Philipp Douschan, Dirk von Lewinski, Philipp Eller, René Schmutz, Uta Kolussi, Fatema Salman, Zainab Ateya, Nafseen Mostafa, Koen De Decker, Niels Van Regenmortel, Anita Jans, Patricia Wijnands, Stefano Coremans, Patrick M. Honore, David De Bels, Tanja Depuydt, Caroline Paillet, Luc-Marie Jacquet, Walter Swinnen, Francis Hannes, Matthia Mergeay, Stijn Van de Velde, Silvie Allaert, Pieter Hoste, Christophe Borin, Sandrine Balon, Vincent Fraipont, Patrick Biston, Nicolas De Schryver, Thierry Dugernier, Ilse Van Cotthem, Vanesa Mercado Telleria, Jasmina Smajic, Angelica Olivetto de Almeida, Silvia Angelica Jorge, Delmiro Becker, Raysa Cristina Schmidt, Evellyn Oliveira, Aline Ramalho, Eliane Mazocoli, Audrey Fioretti, Elaine Barros, Leticia Serpa, Suzana Bianchini, Ticiane Campanili, Taís Pantaleao, Paulo Carlos Garcia, Ana Lucia Vitti Ronchini, Rayanne Santos, Khalid Mahmood Khan Nafees, Nurulhuda Binti A. Manap, Romuald Hentchoya, Sean Bagshaw, Dominic Carney, Sean Bagshaw, Jon Davidow, Sean Bagshaw, Ella Rokosh, Sean Bagshaw, Andréa Maria Laizner, Samantha Smith, Megan McQuirter, Betty Star Kampayana, René Favre, Martin Sills, Andréa Maria Laizner, Julie Dallaire, Andréa Maria Laizner, Cathy Becker, Sherissa Microys, Bonnie Bowes, Jennifer Lajeunesse, Rishi Ghosh, Jacqueline Baptiste-Savoie, Rose Raizman, Sean Bagshaw, Gabriel Suen, Noushin Taghavi, Orla Smith, Clare Fielding, Louise Rose, Julieta Canales, Pia Molina, Javiera Chaparro, Maria Idalia Sepulveda, Matias Jesús Flamm Zamorano, Pamela Rocha, Ximena Villanueva, Paola Araya, Meneses Dayan, Fernando Avalos, Xiaohan Li, Yu Liu, Xinxia Li, Xiaoyan Chen, Zhixia Jiang, Jing Yang, Jingfang Chen, Lei Yang, Kefang Wang, Jie Gao, Xiuhua Fang, Ronghua Zhao, Xinhua Xia, Hongmei Liu, Jing Li, Haiyan Wang, Gen Meng, Yanhong Di, Damei Wang, Rong Hua Zhao, Li Ping Hu, Xiuhua Fang, Xu Peipei, Qing Feng Jiao, Hai Yun Wang, Chun Jie Xia, Yan Liu, Mei Ye, Yan Wan, Wenmei Wang, Yajun Ding, Aiua Ren, Yan Gao, Qi Li, Guifang Du, Jing Yang, Yanling Shen, Yanming Ding, Ning Li, Cui Yuan, Jing Li, Lei Tan, Qiang Lin, Hailing Guo, Howe Yan, Xiao Xu, Wei Zhang, Jinxian Liang, Libing Zhang, Eryun Tian, Qian Zhao, Lin InSu, Jingwen Dong, Yanmei Gu, Ying Liu, Lina Zhao, Wei Wang, Hongmei Qiao, Lili Tuo, Mengmeng Lv, Jin Yu Zhu, JiFen Zhu, Ying Wei, Man Liu, Yin He, Jiyin Cheng, Jin Liu, Na Jia, Dongfang Wei, Qing Li, Xiaoying Wu, Huan Duan, Dongliang Lin, Qiong Liang, Xiaofang Luo, Yunfeng Xiong, Rong Fen Huang, Jing Fu, Tao Zan, Man Ye, Zeya Shi, Yanfei Long, Yang Lei, Xiaodi Liu, Chen Yumei, LingLing Wang, Yali Zhang, Yan Xu, Cheng, Wang Zhijuan, Chengxia Sun, JinHui Song, Yingli Wang, XiuMei Liu, Yupeng Liu, Yuxia Yuan, Qingping Huang, Fengling Yang, Yun Wu, Xianping Luo, Xiaowu Bai, Hong Zheng, Min Song, Yue Sun, ZhangShuangzi Li, Feifei Luo, Miao Liu, Li Chuntang Li, Xinjian Li, Guiping Zhang, Lina Xiao, Tingting Yu, Guangyuan Gao, Wei Wei, Fanglan Wang, Ting Han, Tingting Li, Qi Zeng, Jing Mei Zeng, Yan Long, Fuqun Pan, Jing Wang, Guoxue He, Haiyan Chen, Feifei Zhang, Yu Chao, Gao Chunhua, Xiuying Yao, Dongmei Bai, Lu Liu, Xuelian Xu, Yan Wang, Xuejuan Liang, Na Zhang, Xinxia Li, Aizhi Zhang, Xiaoyan Chen, XiaoChun Hu, Hui Zhang, RuiXia Wang, Poon Shing Tak, Sung Wai Ho, Qun Xia Jiang, Xinran Ding, Liu Hong, Limei Miao, Zhaoxia Feng, LiPing Huang, Juan Wu, Yuping Wang, Jiye Guo, Baoke Zhang, Chaoqun Ma, Yu Han, Congcong Liu, Min Ding, Linlin Luan, Jing Zheng, Shanshan Lv, Shumin Jiang, Wenzhen Cao, Xiujuan Xue, Jing Li, Guangyan Liu, Jing Wang, Xiyan Wei, Wei Zhang, Youru Jiang, Zhiru Yao, Li Gao, Jinhua Li, Wenwen Zhao, Mei Jiang, Junping Hao, Jing Zhang, Caiju Song, Feifei Chen, Shuhui Wang, Lili Hu, Deyan Cao, Yan Liu, Jianhong Wan, Xiaomin Wang, Hongyan Shao, Zhenxia Zhang, Xia Cui, Jingyu Liu, Lijuan Zhao, Xingguo Li, Limei Fan, Ling Zhang, Min Yu, Biyan Li, Chunxia Li, Ling Liu, XueLian Liu, Wenmin Chen, Yan Li, Zhang Zhigang, Wu Yuchen, Chenghau Mu, Guoyan Zhu, Fan Yang, Qi Bo, Ling Li, Meili Chen, Jing Hua Jiang, Hai Yin, Xuelian Pang, Yue Ying Gong, Shunzhu Yang, Xiaoli Yan, Xianhong Zheng, DeHong Lei, Lei Lei, Yinhua Guo, Lihong Liu, Jing Yu, Wei Sun, AiPing Bi, Weiwei Li, Yang Wu, Ji Li, Dongshu Ni, Xiaohan Li, Yu Liu, Zijing Wu, Bing Song, Jingfang Chen, Qin Fei, Yang Xiaoyan, Qiong Ran, Li Xixi, Xueping Jiao, Hua Ji, Sun Zhiping, Ma Hong, Mu Jianhong, Yanhua Hao, Li Yin, Ying Wang, Caihong Hui, Wenjie Ju, Xinhua Xia, Yuxia Huo, Yuxia Wang, Lei Chen, Yan Yan, Qingli Zhao, Hongjuan Chen, Guijun Bao, Ying Cao, Li Hong, Hong Zhang, Ying Zhang, Lina Xu, Jia Guixiang, Ying Li, Hui Min Zhao, Xia Huang, Zhaoxing Dai, Yanman Jian, Hongsu Zhang, Zhixia Tian, Zu Qing Cao, Miao Li, Yang Liu, Fei Ouyang, Fuying Ma, Wangyan Jin, Liuyan Ge, ShiFen Wu, Jing Li, Weilian Yuan, Tianfei Chen, Guanxiu Shi, Zhihong Chen, Kewei Liu, Xue Lin, Ly Yuemen, Sun Lijuan, Xiao Fang Tian, Shuo Wang, ZhangXia Feng, XiaoZhe Liu, Yunchun Dong, Jundi Zhang, Nie Bocui, ZhiXia Jiang, Jing Yang, GuoXian Wang, Yingjuan Zhao, Xiaojun Wu, Qiao Yang, Rongjun Ling Hu, Xue Qin Li, Zhu Jun Yu, Yanlan Yao, Xiaoqiong Deng, Yan Xiao, Yan Xie, Yanping Yang, Huai Yang, Yuming Zhou, Zhuqing Li, Min Xiao, YongXia Yang, Yani Tian, Luz Marina Silva Gama, Juan Sebastian Hernandez, Yenny Cardenas, Nestor Caicedo, Jorge Marin, Maria-Elena Ochoa, Monica Gomez, José Rojas-Suarez, Jeniffer Gonzalez, Amylkar José Garay Reyes, Edwin Chapeta, Estefania Orozco, Ina Filipović-Grčić, Anita Vuković, Suzana Pečenković, Aleksandar Šuput, Alan Sustic, Gordana Zivanovic-Posilovic, Armanda Bozena, Nikolina Udiljak, Morena Milic, Renata Curic Radivojevic, Slobodan Mihaljevic, Marijana Matas, Dinko Tonkovic, Hemena Čuljak, Ivana Herceg, Gordana Pavlisa, Milena Dobric, Tatjana Beker, Višnja Nesek Adam, Tanja Goranovic, Chrysanthos Markoulias, Mina Mathaios, Maria Mylordou, Eleni Achilleos, Pavlina Kleanthous, Veronika Kotanidi, Maria Foka, Iwy Charalabous, Anna Alexandrou, Marios Georgiou, Artemis Patsalos, Sofia Zepoy, Constantina Constantinou, Petr Piza, Tomas Vymazal, Elisabeth Wiborg, Louise Bruhn, Karin Kaasby, Karin Rehnholt Pedersen, Sanne Mikkelsen, Marie Collet, Anne Langvad, Hanne Andresen, Susanne Fischer, Inger Ebbesen Kjærgård, Britta Jepsen, Birthe Husted, Morten Bestle, Anne Marie Kodal, Tina Charlotte Bitsch Hansen, Anne Sofie Bomholt Pedersen, Tina Damgaar Thomsen, Anisette Hoegenhaven, Mette From, Tine Melgaard Frandsen, Grit Henning, Anja Hansen, Hanne Irene Jensen, Inger Abildgaard Bliksted, Luis Mario Tamayo, Pedro Mogrovejo, Hernan Aguirre-Bermeo, Carolina Palaez, Diego Rolando Morocho Tutillo, Cintia Valencia Hurtado, Maria Fernanda García, Diana Alvarez, Fausto Guerrero, Alexandra Vasquez, Martin Kütimets, Kadri Tamme, Liivi Maddison, Eneli Anvelt, Lomangisi Dlamini-Sserumaga, Carita Löfqvist, Virpi Lusenius, Outi Kauppi, Jenni-Katarina Sakki, Tarja Tervo-Heikkinen, Ulla Kesti, Merja Merilainen, Elina Karjula, Minna Peltomaa, Auli Palmu, Maarit Ahtiala, Maija Anniina Valta, Hervé Mentec, Gaëtan Plantefève, Guillaume Besch, Sébastien Pili-Floury, Stanislas Ledochowski, Marc Danguy des Déserts, Christophe Giacardi, Cédric Daubin, Audrey Massard, Yann Le Guen, Agnès Blanc, Simon Mandaroux, Silvia Calvino Günther, Prune Avogadro, Anthony Radavidson, Jean Turc, Sébastien Jochmans, Hervé Quintard, Laetitia Boyer, Cédric Bruel, François Philippart, Philippe Montravers, Enora Atchade, Nadine Flessel, Benoît Chinardet, Léa Soulisse, Cindy Pillard, Delphine Ngo, Benjamin Bongiorno, Nathalie Heitzler, Virginie Souppart, Nathalie Gautheret, Jean-Francois Timsit, Fatiha Essardy, Muriel Fartoukh, Daisy Mehay, Fabienne Etourneau, Jean-christophe Farkas, Pascal Beuret, Gabriel Preda, Etienne De Montmollin, Vincent Castelain, Ulrich Jaschinski, Monika Rothenfusser, Detlef Kindgen-Milles, Thomas Dimski, Christine Fiedler, Tobias Heinicke, Patrick Meybohm, Tobias Schulze, Marc Bota, Sabrina Pelz, Tobias Odenthal, Martin Christ, Frank Bloos, Kathrin Bösl, Achilleas Chovas, Sebastian Stehr, Philipp Simon, Sarah Grotheer, Sebastian Schüppel, Stefan Schaller, Lea Albrecht, Andeas Stübner, Stephan Graeser, Nina Kolbe, Martina Lausch, Anja Diers, Ulf Guenther, Reimer Riessen, Martin Roller, Irene Pearl Osei, Anita-Chrysolyte Kusi-Appiah, Yakubu H. Yakubu, Belinda Guadi-Gosh, Christos Dragoumanis, Christos Christofis, Nikolaos Kazakos, Styliani Bastani, Charalampos Martinos, Vasileios Bekos, Metaxia Papanikolaou, Theonymfi Papavasilopoulou, Anna Efthymiou, Vasiliki Chantziara, Anna Kyriakoudi, Nikolaos Kakaras, Chrisi Diakaki, Aikaterini Flevari, Charikleia Nikolaou, Kounougeri Katerina, Lamprini Avramopoulou, Kyriaki Tsikritsaki, Georgios Gkiokas, Eirini Pantiora, Chrysostomos Katsenos, Eirini-Chysovalanto Patsiou, Paraskevi Alexandropoulou, Ioannis Koutsodimitropoulos, Epaminontas Farmakis, Konstantina Nestora, Marinos Chatzis, Eumorfia Kondili, Stella Soundoulounaki, Ourania Mousafiri, Dimitra Lepida, Antonia Liarmakopoulou, Vasilios Koulouras, Georgios Papathanakos, Mrina Oikonomou, Panagiotis Ioannides, Dimitrios Papadopoulos, Ioannis Staikos, Maria Stafylaraki, Bogdan Raitsiou, Konstantinos Mandis, Ifigenia Ravani, Styliani Kourelea, Aikaterini Efthimiou, Giannoula Thoma, Apostolos Bakas, Konstantinos Psarulis, Souzana Anisoglou, Eirini Papageorgiou, Evangelia Michailidou, Thomai Tholioti, Athena Lavrentieva, Evdokia Sourla, Anastasia Spyropoulou, Nikolaos Pantelas, Kristina Mariana Matei Stalika, Ioannis Georgakas, Antigoni Karathanou, Syragoula Tsikriki, Aikaterini Dimoula, Sofia Kanakaki, Aristeidis Vakalos, Konstantinos Pagioulas, Judy Enamorado Enamorado, Gabor Nardai, Fatime Hawchar, Asbjorn Blondal, Brynja Rygvadottir, Rannveig J. Jonasdottir, Hrönn Birgisdottir, Bhagyesh Shah, Shuchi Kaushik, Swagata Tripathy, Mukta Singh, Sonika Agarwal, Manish Gupta, Meraj Ahmad, Kishore Mangal, Vaibhav Bhargava, Vilas Kushare, Simant Jha, Lakshay Bhakhtiani, Amit Gupta, Manoj Kamal, Mohan Gurjar, Arvind Baronia, Bram Kilapong, Ade Susanti, Mayang Indah Lestari, Zulkifli Zulkifli, Windu Baskoro, Farid Zand, Fatemeh Zarei, Ata Mahmoodpoor, Farshad Heidari, Fateme Jafaraghaee, Aidan O’Shea, Fiona O’Shea, Caroline O’Donnell, Geraldine Craig, Gerry Fitzpatrick, Lisa Dunne, Jennifer Hastings, Brian Marsh, Caitriona Cody, Elizabeth Campbell, Deirdre Doyle, Michelle Pacturanan, Christine Sheehan, Annette Carey, Charlotte Carter, Regina Mulvey, Damien O’Connell Rosemary Finn, Catherine Motherway, Amy Walsh, Jennifer Kehoe, Shella Delossantos, Jennifer Lalor, Siobhan O’Nuallain, Helena Behan, Sandra McPherson, Ailesh Corcoran, Patricia Gordon, Glenda Rooney, Dassy Levy, Mazal Azencot, Julie Benbenishty, Vladimir Gurevich, Alinoy Lavy, Valentina Bendelari, Romina Marconi, Antonio Barone, Chiara Gatti, Andrea Giampaoletti, Cinzia Borgognoni, Davide Massimo Ghioldi, Arena Raimondo, Giacomo Castiglione, Anna Vita Bruno, Giorgia Rubulotta, Antonella Mo, Amalia Corso, Salvatore Girianni, Andrea Bruni, Eugenio Garofalo, Salvatore Maurizio Maggiore, Alessandro Di Risio, Italo Calamai, Rosario Spina, Savino Spadaro, Carlo Alberto Volta, Antonella Cotoia, Lucia Mirabella, Laura Maulicino, Giancarlo Abregal, Maria Donvito, Paolo D’Ambrosio, Filipo Binda, Ileana Adamina, Alessandro Galazzi, Alessandra Negro, Rosanna Vaschetto, Fabio Capuzzi, Margherita Boschetto, Lucia Stivanello, Luciano Bonaccorso, Chiara Megna, Andrea Cortegiani, Pasquale Iozzo, Antonino Rizzo, Giovanni Scire, Maria Rosa Taibi, Francesca Paola Tranello, Antonio Manzo, Lidia Traina, Beatrice Pastore, Attilio Quaini, Gian Domenico Giusti, Gloria Montaldi, Federica Piergentili, Federica Mancini, Simona Casaioli, Francesco Uccelli, Fabio Guarracino, Adriana Onelli, Valentina Di Gravio, Maria Cossu, Oliva Matrona, Monica Rocco, Daniela Alampi, Federica Dellafiore, Flavia Ranalli, Matteo Bossolasco, Elisabetta Brizio, Pina Migliorino, Paolo Cortellazi, Moris Rosati, Francesco D’Ambrosio, Catia Quagliotto, Erik Roman-Pognuz, Alberto Peratoner, Silvia De Rosa, Marina Alessandra Martin, Francesca De Sanctis, Paolo Ciorba, Kelly Fletcher, Patrick Toppin, Hyacinth Harding-Goldson, Shunsuke Taito, Nobuaki Shime, Ryohey Yamamoto, Fumiya Kanda, Akemi Hirao, Moritoki Egi, Ayako Noguchi, Satoru Hashimoto, Umeda Aya, Hideaki Sakuramoto, Akira Ohuchi, Jun Kataoka, Kumi Maruyama, Izumi Nakayama, Yoshimasa Nishime, Koji Fujimoto, Kenji Takahashi, Mayumi Tsujimoto, Masako Shimizu, Wangari Waweru-Siika, Eunice Tole, Malcolm C. Correia, Je Hyeong Kim, Sunghoon Park, Kyung Chan Kim, Jonghyun Baek, Jung-Min Bae, So Young Park, Tai Sun Park, Heung Bum Lee, Seung Yong Park, Jisoo Park, Lee Yeon-Joo, Cho Young-Jae, Sang-Miin Lee, Kyeongman Jeon, Seok Chan Kim, Jongmin Lee, Hyun Keun Chee, Jin Won Huh, Yun Su Sim, Junghyun Kim, Youjin Chang, Jong-Joon Ahn, Byung Ju Kang, Won-Yeon Lee, Seok Jeong Lee, Burhan Hadri, Nehat Baftiu, Ivasr Krastins, Mihails Dolgusevs, Fayez François Abillama, Sonia Stiban, Michel El Feghaly, Elie Gharios, Marie Merheb, Mohamed Benlamin, Ala Khaled, Wesal Ali Belkhair, Majd Tabib, Firas Ashour, Ahmed Elhadi, Osama Wanees Emhemid Tababa, Taha Khaled, Soad Imhmed R. Alkhumsi, Abdualhamid I Alshrif, Ahmed Ali Aboufray, Aya Alabuzidi, Ahmed Ramadan Triki, Mala Elgammudi, Hajer Ben Zahra, Enas Soula, Maram Milud Said Al-Alawi, Hazem Ahmed, Mohamed Abdurazzag Ali Ghula, Saulius Vosylius, Lucie Mouton, Touraj Rastegar, Claude Sertznig, Gilles Martin, Cyril Thix, Christian Theisen, Christian Ferretti, Fränk Gils, Marc Gallion, Asmah Zainudin, Laila Kamaliah Kamalul Bahrin, Shanti Rudra Deva, Azmin Huda Abdul Rahim, Sherliza Wahab, Mohd Zulfakar Mazlan, W. Nazaruddin W. Hassan, Wan Nasrudin Wan Ismail, Mohd Nazri Ali, Tien Meng Khoo, Noryani Mohd Samat, Jenny May Geok Tong, Nik Azman Nik Adib, Mohd Basri Mat Nor, Shanthi Ratnam, Nahla Ismail, Shanthi Ratnam, Siti Rohayah Sulaiman, Kit Weng Foong, Anita Alias, Ngu Pei Hua, Sundaresan Maiyalagan, Sundaresan Maiyalagan, Jorge Macias Zermeno, Daniel Blanco, Karely Duran, Claudia Lizbeth Lopez Nava, San Juan Roman Nandyelly, Luis Alejandro Sanchez-Hurtado, Brigitte Tejeda-Huezo, Mario Del Moral Armengol, Luis Pedro Ambriz Nava, Jorge Guerra Herrera, Gilberto Felipe Vazquez de Anda, Humberto Gallegos-Perez, Nancy Hernandez-Sanchez, Lucia Hernandez-Ponce, Luis Gorordo-Delsol, Marcos Hernandez-Romero, Saira Gomez, Fernando Molinar, Silvio A. Ñamendys-Silva, Juan P. Romero-Gonzalez, Daira Gonzalez, Antonio Landaverde, Miguel Ángel Sosa, Berenice Navarro, José Ivan Rodriguez de Molina Serrano, Sergio Reyes Iburrigarro, Alejandro Ibarra, Joaquin Aguirre, Mayra Martinez-Gonzalez, Nayeli Rocio Cañas Padilla, Ana Alícia Velarde Pineda, Missael Vladimir Espinoza Villafuerte, María Ocotlan Gonzalez Herrera, Adrian Belii, Mendsaikhan Naranpurev, Battsetseg Baasanjav, Abdelhamid Hachimi, Mina Elkhayari, Khalid Abidi, Tarek Dendane, Nisha Bhandari Subedi, Sabina Dhakal Pathak, Prabha Gautam, Meena Manandhar, Laura Van Gulik, Mark Van Den Brink, Peter Van Vliet, Benjamin Gerretsen, Lettie Van Den Berg, Marina De Haan, Binny Tuinstra, Paul Kuijpers, Jennifer Reijntjens, Jan Wytze Vermeijden, Martin Rinket, Margijske Vanroest, Auke Reidinga, Bert Loef, Willem Dieperink, Marisa Onrust, Tom Dormans, Laura Bormans, Matty Koopmans, Rik T. Gerritsen, Arlette Van Den Elst, Mirjam Evers, Oscar Oiting, Rob Wilting, Bart Ramaker, Mark van der Kuil, Jan-Willem Fijen, Lenneke Haas, Dylan De Lange, Jasper Haringman, Lynette Newby, Rachael Parke, Eileen Gilder, Danielle Hacking, Rica Dagooc, Rima Song, Hansjoerg Waibel, Frances Dawn, Jackie Rapley, Llesley Chadwick, Carmel Chapman, Petra Crone, Jonathan Albrett, Peter Marko, Jennifer Goodson, Troy Browne, Richard Whitticase, Cheryl Davidson, Harriet Judd, Daniel Owens, Tonia Onyeka, Innocent Ugwu, Rose Ilesanmi, Prisca Olabisi Adejumo, Afolabi Owojuyigbe, Anthony Adenekan, Stella Uba, Christiana Chime, Deborah Jibrin, Babangida John Sankey, Oyebola Adekola, Simeon Olanipekun, Simeon Olanipekun, Oyebola Adekola, Mirjana Shosolcheva, Vanja Gievski, Andrijan Kartalov, Filip Naumovski, Biljana Kuzmanovska, Angela Trposak, Zaneta Bogoevska-Miteva, Rodney Rosalia, Brita Fosser Olsen, Britt Sjobo, Karianne Dale Jensen, Drammen Sykehus, Birgitte Fosser Johansen, Esben Straede, Edda Johansen, Inger Johanne Finnstrom, Annette Toellefsen, Hege Ostenjo, Hege Bjorgen, Bjorn Bratsberg, Elin Kristoffersen, Elin Mari Skorstad, Siri Hansen, Sylvi Vullum, Gro Anne Lunde, Wenche Arntsen, Mette Lund, Gro Ringstad Akselsen, Kristina Reinertsen Monstad, Ane Stenset, Hanne Haugom, Bjoern Monsen, Lisa Høgvall, Siw Trudvang, Britt Galaaen, Siv Karin Malmin, Marit Hildegunn Andersen, Rita Foss Hargott, Yvonne Andersen, Elin Steffenak, Marit Nyhus, Barbro Meland, Madiha Hashmi, Noelia Rivas, Elizabeth Maidana, Alberto de Jesús Ortiz, Dolly Mabel Bordon Cabral, Marcelo Simi, Cesar Aponte, Juan Carlos Rivas, Sirley Gill, Amilcar Garcia, Gloria Alvarenga, Laura Cespedes, Hugo Perez, Maria Liz Moreira, Fidelina Canete, Roberto Gonzalez, Natalia Monges, Amilcar Garcia, Mary Coman, Marcelo Pederzani, Natalia Franco, Ferdinand Aganon, Regina Martinez, Debbie Noblezada-Uy, Chris Gerome Ellazar, Franklin Dean Cerezo, Aaron Mark Hernandez, Jose Emmanuel Palo, Cristal April Jane Aperocho, Michael Isanan, Marta Tubacka, Przemyslaw Jasiewicz, Miroslaw Czuczwar, Michal Borys, Aleksandra Gutysz-Wojnicka, Lidia Glinka, Ryszard Gawda, Malgorzata Mikaszewska-Sokolewicz, Jan Bilawicz, Paula Cabrita, João Vieira, Margarida Ferreira Figueiredo, Cristiana Mota Pinheiro, Nelson Antunes, Laura Pedro, Fatima Ferreira, Isabel Parente, Maria Varela, Fatima Fernandes, Claudia Martins, Abel Viveiros, Raquel Cavaco, Clara Santa Rita, Sofia Dias, Ana Margarida Feranandes, Pedro Silva, Catarina Nunes, João Cabral, Bruno Sousa, Filpe Pires, Hilaryano Ferreira, Jacinta Santos, Vitor Manuel Vaz Pinto, Bruno Miguel Bispo, Amelia Ferreira, Elena Molinos, Estevão Lafuente, Ricardo Gregorio, Humberto Costa, Ângela Lima, Susana Ferreira, Vanda Seromenho, Eulália Luis, Idália Valerio, Helena Cesar, Ana Tavares, Ahmed Subhy Alsheikhly, Saeed Mahmood, Catalin Traian Guran, Alida Moise, Daniela Carmen Filipescu, Mihail Luchian, Dana Tomescu, Mihai Popescu, Monica Adriana Scutariu, Cristina Petrisor, Natalia Hagau, Ioana Grigoras, Tatiana Patrichi, Vitaly Gusarev, Alexandra Pivkina, Vladimir Kulakov, Olga Ignatenko, Julia Kovaleva, Trina Zhivotneva, Marina Zhedaeva, Nikita Matiushkov, Olga Ershova, Natalya Egorova, Victoria Khoronenko, Danil Baskakov, Dmitry Sergeev, Michael Piradov, Liudmila Grishina, Marat Magomedov, Evgeniy Zuev, Uri Gorokhovatsky, Anna Leonova, Liudmila Fadeeva, Vladislav Belskiy, Dmitriy Galishevskiy, Nadezhda Zubareva, Maksim Tribulev, Oksana Zueva, Alexander Kiselev, Nikolaj Kamenshchikov, Ekaterina Tokareva, Maxim Petrushin, Irina Starchenko, Theogene Twagirumugabe, Isaac Nshimyumuremyi, Jerome Muhizi, Egide Buregeya, Josue Nzarora, Amer Assiri, Maie Salem Ebaid, Ghaleb Almekhlafi, Yasser Mandourah, Jelena Velickovic, Dejan Veličković, Bojan Jovanovic, Adi Hadzibegovic, Branislava Stefanovic, Vanja Misic, Vesna Bumbasirevic, Marija Rajković, Radmilo Jankovic, Milena Stojanovic, Srđan Gavrilovic, Maja Stanojević, Andrea Martonova, Aktham Yaghi, Anton Turčan, Peter Firment, Garri Slobodianiuk, Daria Rabarova, Danca Lančaričová, Janko Vlaovic, Matjaž Groznik, Milica Lukic, Janja Perme, Maja Sostaric, Nejc Umek, Tomislav Mirkovic, Simon Dolenc, Rihard Knafelj, Misa Fister, Nika Zorko, Andrej Markota, Nomhle Princess Yeni, Phumele Jali, Shelley Schmollgruber, Muhommed Ridwaan Syed, Nivisha Parag, Robert Wise, Maria Galiana, José Alejandro Navarro, Ana María De Pablo, Patricia Albert, Pilar Martinez, Yolanda Mendiara, Barbara Garcia, Ana Alabart Llinas, Marilyn Riveiro, Elisabet Gallart, Alba Riera, Miquel Sanz, Swagotika Salo, Miguel Angel Gimenez Lajara, Montserrat Venturas Nieto, Rosa Garcia, José Manuel Garcia Pena, Maria Carmen Gorgolas, Maria Aranzazu Isasi, Rafael Sierra, Federico Gordo, Isabel Conejo, Vicent Salvà-Costa, Carolina Garzón-Tovar, Sara Lospitao, Rafael Gonzalez, Pedro Gutierrez, Mercè Girona, Jordi Adamuz, Pablo Garcia Olivares, José Peral Gutierrez de Ceballos, Celia Tirado, Irene De Wit, Ana Belén Curto Polo, Maria del Mar Diaz Salcedo, Javier Ripolles-Melchor, Eugenio Martinez-Hurtado, Jorge Duerto Alvarez, María Luisa Bravo Arcas, Juan Ignacio Torres Gonzalez, Ana Belén Sánchez de la Ventana, Pablo Lopez-Arcas Calleja, Raquel Garcia Alvarez, Purificacion Sanchez Zamora, Alvaro Ortega Guerrero, Rosario Cosano, Jonathan Perez-Vacas, Margarita Campos-Perez, Emma Moreno Barreiro, Losune Cano Sanchez, Monica Garcia Diaz, Raquel Jimenez, Lorena Del Rio Cabajo, Daniel Sancho Muriel, Helena Fernandez Alonso, Ana Wensell Fernández, Isabel Santín Piñan, Guillermo Muñiz Albaiceta, Maria Cristina Iglesias Fernandez, Francisco Javier Saenz Abos, Pablo Monedero, Ramon Molina Chueca, Lydia Gallego Aguirre, Silvia Call Manosa, Carmen Partera Luque, Neus Calpe, Monica Recio Losilla, Meritxell Tapia Fores, Olga Farre, Oscar Fernandez, M. del Rosario Villar Redondo, Donaldo S. Arteta Arteta, Maria Angeles Hurtado Sanchez, Cristina Paños Espinosa, Laura Martinez Reyes, Laura Claramunt Domenech, Carmen Velasco Guillén, Josep Trenado Alvarez, Mercedes del Cotillo, Jesus Emilio Barrueco-Francioni, Belen Burgos Conde, Maria Pilar Sogues Blanco, Maria Luisa Blasco, Ana Isabel Clement, Clara Hurtado, Luz Coronado Sanz, David Perez-Torres, Estefanía Prol-Silva, Jorge Pereira, Iván Areán González, Anastasio Espejo Cano, Cesar Rodriguez Nuñez, Inmaculada Lorenzo Fernadez, Alejandra Azahara Marguello Fernandez, Rosa Del Bosque Diez, Badiola Hilario, Begoña Zalba-Etayo, Ana Pascual-Bielsa, Bernardo Panka, Preveen Banwarie, Dick Nahar, Alisha van Axel, Naraindath N. Boedjawan, Erika Backlund Jansson, Ann-Sofie Malvemyr, Lotta Johansson, Ulla Sandberg, Catarina Tingsvik, Gunilla Mattsson, Gun Löf, Martin Spångfors, Mona Ringdal, Sebastian Geijer, Lotti Orvelius, Mia Hylen, Caroline Lagerhäll, Eva Joelsson-Alm, Eva Åkerman, Viveca Hamback Hellkvist, Ulrica Mickelsson, Eva Åkerman, Ewa Wahlbom, Ing-Marie Larsson, Ewa Wallin, Filippo Boroli, Solenne Ory, Joerg C. Schefold, Margaret Lynn Jong, Alexander Dullenkopf, Martin Lang, Yvan Fleury, Marianne Maus, Nawfel Ben-Hamouda, Anne Fishman, Mei Yu Hsu, Shu Chuan Chang, Konlawij Trongtratul, Chaiwut Sawawiboon, Sunthiti Morakul, Bodin Khwannimit, Lorna Merritt-Charles, Keevan Singh, Dale Ventour, Dianne Figaro-Barclay, Sasha Sankar-Maharaj, Mhamed Sami Mebazaa, Salma Kamoun, Souheil Elatrous, Lamia Besbes, Fekri Abroug, Walid Naija, Youssef Zied Elhechmi, Walid Sellami, Zied Hajjej, Takoua Merhabene, Imen Talik, Ozlem Ozkan Kuscu, Ozcengiz Dilek, Avşar Zerman, Hayriye Cankar Dal, Sema Turan, Semih Aydemir, Hakan Yilmaz, Duygu Kayar Calili, Seval İzdes, Melike Cengiz, Ayça Gümüş, Banu Taşdemir, Ali Kağnıcı, Mustafa Ay, Serap Avcı Ay, Gulbahar Caliskan, Turkay Akbas, Abidin Oner Balbay, Serdar Efe, Volkan Inal, Gülseren Elay, Pınar Karabacak, Boğaç Özserezli, Evren Şentürk, Oktay Demirkiran, Suha Bozbay, Yalım Dikmen, Elif Erdogan, Mustafa Akker, Nebia Peker, Asu Ozgultekin, Sibel Ocak Serin, Can Turan, Gulsah Karaoren, Senay Goksu, Sait Karakurt, Huseyin Arikan, Fethi Gül, İsmail Cinel, Iskender Kara, Hasan Nabi Undar, Yesim Serife Bayraktar, Jale Bengi Çelik, Murat Emre Tokur, Demet Tok Aydin, İsmail Yildiz, Beysim Özcan, Başar Erdivanli, Başar Erdivanli, Beysim Özcan, Ahmet Eroglu, Devrim Akdağ, Nurdan Ünlü, Mark Fielding, Adonis Dungca, Ashwaq Ali, Bindu Thankamma, Paul Eric Reyes, Sini John, Ajitha Rajendran, Fatima Kasem El Ahmad, Kathleen Ann Smiley, Susanna Hojden, Mia Thorning Miller, Vishnu Das Sasidharan Nair, Maria Gracia San Antonio, Khaled Al Qawasmeh, Sabah Abu Shawish, Hilary Twiggs, Ines Rosado, Volodymyr Babych, Faye Morren, Charlotte Young, Nicola Vaughan-Jones, Stephanie Harris, Karen Burns, Carmel Georgiev, Rosina Shayamano, Ian Kerslake, Peter Creber, Ana Vochin, Catherine O’Brien, Paul Caddell, Samantha Hagan, Mandy Hughes, Tomasz Torlinski, James Sherwin, Santhana Kannan, Amber Markham, Richard Lebon, Jason Cupitt, Julius Cranshaw, Nigel White, Victoria Marriott, Wendy Milner, Casiano Barrera Groba, Joao Azoia, Petra Polgarova, Shaly George, Ritoo Kapoor, Ceri Lynch, Nathalie Fox, Karen Cranmer, Natalie Fox, Thomas Llewellym, Kelly Matthews, Louise Maltby, Jowena Ibao, Karen Boulton, Rachel Jarman, Karen Baxter, Ashok Sundai Raj, Arif Moghal, Joanne White, Suzanne Barrowcliffe, Mark Pulletz, Vaarisan Ganeshalingam, Rosaleen Baruah, Carole Boulanger, Helen Baker, Justin Woods, Poe Poe Ei, Vongayi Ogbeide, Paul Hayden, Kelly Matthews, Jennifer Hughes, Madhu Balasubramanian, Armorel Salberg, Rajnish Saha, Dagmar Holmquist, Charlotte Young, Claire Derbyshire, Neil Smith, Elizabeth Stones, Jane Ademokun, Monica Popescu, Maria Schofield Legorburo, Samantha North, Carole Brett, Helen Jaundoo, Jayne Craig, Simon Whiteley, Clare Howcroft, Liz Wilby, Peter Delve, David Shaw, Karen Williams, Ingeborg D. Welters, Jane McMullen, Stephen Brett, Leah Flores, Treiza Trueman-Dawkins, Francesca Rubulotta, Mae Templeton, John Adams, Catherine Smith, John Prowle, Heather Byers, Andrea McDonnell, Bernd Oliver Rose, Rosie Reece-Anthony, Luis Mendes, Marcela Vizcaychipi, Rhian Bull, Grace Lacaden, Eleanor Santiago, Carlos Castro Delgado, Sarah Farnell-Ward, Elaine Thorpe, Justine Somerville, Anne Williams, Donna Cummings, Helen Derrick, Sarah Brumwell, Claire Randell, Nicola McCann, Emma Aves, Gillian Berry, Tamas Szakmany, Una Gunter, Paul Pulak, Nikki Sarkar, Kerry Wright, Vitor Gomes, Jo Jones, Ruth Palfrey, Julie Camsooksai, Abby Lewis, Antony Eneas, Ascanio Tridente, Louise Barr, Tomas Jovaisa, Beverley Thomas, Emma Parkin, Daniel Horner, Christian Frey, Suzanne Bench, Rachel Baumber, Phil Broadhurst, Matthew Jackson, Lynne Williams, Michele Clark, Jonathan Paddle, Sarah Bean, Sarah Buckley, Christopher Palfreeman, Sophie Liu, Nicola Allison, Ben Attwood, Penny Parsons, Victoria Houghton, Sarah Jane Turner, David Higgins, Egidija Bielskute, Nicola Horrigan, Reni Jacob, Karen Habgood, Ahmed Zaki, Amy Collins, Jenny Lord, Charalice Ramiro, Agnieszka Kubisz-Pudelko, Michelle Kotze, Helen Williams, Ihor Iovenko, Alexander Tsarev, Lesia Zgrzheblovska, Arturo Briva, Gabriela Mendez, Lena Napolitano, Leif Saager, Magnus Teig, Jarone Lee, Gabriel Enrique Rodriguez, Talia Ben-Jacob, Christopher Potestio, Timothy Eng, Dea Mahanes, Ashish Khanna, Abhijit Duggal, Masakatsu Nananmori, Manuel Lois, Anna Diaz, Kunal Karamchandani, Cheryl Bealer, Cindy Barefield, Dorothy Terry, Pauline Fivecoat, Olakunle Idowu, Juan Cata, Tara Clesi, Jessica Peterson, Kevin Hatton, Jasdeep Dhaliwal, Dorothee Mueller, Jing Tao, Ashley Szabo Eltorai, Stephen M. Pastores, Natalie Remor, Janel Salazar, Javier Bogarin, Diane Barkas, Aaron Joffe, Christopher Barnes, Christopher Barnes, Carrie Sona, Marilyn Schallom, Jack Short, Javier Lorenzo, Ingrid Von Der Osten, Marta Borkowska, Mireia Llaurado-Serra, Liesbet Demarré, Vincianne Pleitinckx, Frances Lin, Cynthia Xing, Jing Li, Anne-Sophie Debue, Stefan Goller, Andrea Cortegiani, Chiara Megna, Elsa Afonso, V. Gusarov, Eugeniya Larina, M. Llaurado-Serra, Konlawij Trongtrakul, Yalim Dikmen, and Elif Erdogan
References
- 1.National Pressure Injury Advisory Panel, European Pressure Ulcer Advisory Panel, and Pan Pacific Pressure Injury Alliance . Prevention and treatment of pressure ulcers: Clinical practice guideline. Osborne Park: Cambridge Media; 2019. [Google Scholar]
- 2.National Pressure Ulcer Advisory Panel, European Pressure Ulcer Advisory Panel, and Pan Pacific Pressure Injury Alliance . Prevention and treatment of pressure ulcers: clinical practice guideline. Osborne Park: Cambridge Media; 2014. [Google Scholar]
- 3.Edsberg LE, Black JM, Goldberg M, McNichol L, Moore L, Sieggreen M. Revised National Pressure Ulcer Advisory Panel pressure injury staging system: revised pressure injury staging system. J Wound Ostomy Cont Nurs. 2016;43:585–597. doi: 10.1097/WON.0000000000000281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.National Pressure Ulcer Advisory Panel (2017) NPUAP position statement on staging—2017 clarifications. https://npuap.org/page/PositionStatements. Accessed 25 Aug 2019
- 5.Gefen A (2008) How much time does it take to get a pressure ulcer? Integrated evidence from human, animal, and in vitro studies. Ostomy Wound Manag 54:26–28, 30-25 [PubMed]
- 6.Gorecki C, Brown JM, Nelson EA, et al. Impact of pressure ulcers on quality of life in older patients: a systematic review. J Am Geriatr Soc. 2009;57:1175–1183. doi: 10.1111/j.1532-5415.2009.02307.x. [DOI] [PubMed] [Google Scholar]
- 7.Dealey C, Posnett J, Walker A (2012) The cost of pressure ulcers in the United Kingdom. J Wound Care 21:261–262, 264, 266 [DOI] [PubMed]
- 8.Demarré L, Van Lancker A, Van Hecke A, et al. The cost of prevention and treatment of pressure ulcers: a systematic review. Int J Nurs Stud. 2015;52:1754–1774. doi: 10.1016/j.ijnurstu.2015.06.006. [DOI] [PubMed] [Google Scholar]
- 9.Guest JF, Ayoub N, McIlwraith T, et al. Health economic burden that different wound types impose on the UK’s National Health Service. Int Wound J. 2017;14:322–330. doi: 10.1111/iwj.12603. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Nguyen KH, Chaboyer W, Whitty JA. Pressure injury in Australian public hospitals: a cost-of-illness study. Aust Health Rev. 2015;39:329–336. doi: 10.1071/AH14088. [DOI] [PubMed] [Google Scholar]
- 11.Padula WV, Delarmente BA. The national cost of hospital-acquired pressure injuries in the United States. Int Wound J. 2019;16:634–640. doi: 10.1111/iwj.13071. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Cox J. Pressure injury risk factors in adult critical care patients: a review of the literature. Ostomy Wound Manag. 2017;63:30–43. doi: 10.25270/owm.2017.08.3043. [DOI] [PubMed] [Google Scholar]
- 13.Coyer F, Miles S, Gosley S, et al. Pressure injury prevalence in intensive care versus non-intensive care patients: a state-wide comparison. Aust Crit Care. 2017;30:244–250. doi: 10.1016/j.aucc.2016.12.003. [DOI] [PubMed] [Google Scholar]
- 14.Soodmand M, Moghadamnia MT, Aghaei I, Ghasemzadeh G, Lili EK, Rad EH. Effects of hemodynamic factors and oxygenation on the incidence of pressure ulcers in the ICU. Adv Skin Wound Care. 2019;32:359–364. doi: 10.1097/01.ASW.0000553599.20444.f4. [DOI] [PubMed] [Google Scholar]
- 15.Barakat-Johnson M, Lai M, Wand T, Li MB, White K, Coyer F. The incidence and prevalence of medical device-related pressure ulcers in intensive care: a systematic review. J Wound Care. 2019;28:512–521. doi: 10.12968/jowc.2019.28.8.512. [DOI] [PubMed] [Google Scholar]
- 16.Kahn JM, Le T, Angus DC, Cox CE, et al. The epidemiology of chronic critical illness in the United States. Crit Care Med. 2015;43:282–287. doi: 10.1097/CCM.0000000000000710. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Flaatten H, de Lange DW, Artigas A, et al. The status of intensive care medicine research and a future agenda for very old patients in the ICU. Intensive Care Med. 2017;43:1319–1328. doi: 10.1007/s00134-017-4718-z. [DOI] [PubMed] [Google Scholar]
- 18.Laporte L, Hermetet C, Jouan Y, et al. Ten-year trends in intensive care admissions for respiratory infections in the elderly. Ann Intensive Care. 2018;8(1):84. doi: 10.1186/s13613-018-0430-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Llaurado-Serra M, Afonso E. Pressure injuries in intensive care: what is new? Intensive Crit Care Nurs. 2018;45:3–5. doi: 10.1016/j.iccn.2017.12.002. [DOI] [PubMed] [Google Scholar]
- 20.Chaboyer WP, Thalib L, Harbeck EL, et al. Incidence and prevalence of pressure injuries in adult intensive care patients: a systematic review and meta-analysis. Crit Care Med. 2018;46:e1074–e1081. doi: 10.1097/CCM.0000000000003366. [DOI] [PubMed] [Google Scholar]
- 21.Le Gall J-R, Lemeshow S, Saulnier F. A new Simplified Acute Physiology Score (SAPS II) based on a European/North American multicenter study. JAMA. 1993;270:2957–2963. doi: 10.1001/jama.1993.03510240069035. [DOI] [PubMed] [Google Scholar]
- 22.Bergstrom N, Braden B, Laquzza A, Holman V. The Braden scale for predicting pressure sore risk—reliability studies. Nurs Res. 1985;34:383. [PubMed] [Google Scholar]
- 23.R Core Team . R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2018. [Google Scholar]
- 24.Alderden J, Rondinelli J, Pepper G, Cummins M, Whitney J. Risk factors for pressure injuries among critical care patients: a systematic review. Int J Nurs Stud. 2017;71:97–114. doi: 10.1016/j.ijnurstu.2017.03.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Lima Serrano M, González Méndez MI, Carrasco Cebollero FM, Lima Rodríguez JS. Risk factors for pressure ulcer development in Intensive Care Units: a systematic review. Med Intensiva. 2017;41:339–346. doi: 10.1016/j.medin.2016.09.003. [DOI] [PubMed] [Google Scholar]
- 26.Sala JJ, Mayampurath A, Solmos S, et al. Predictors of pressure injury development in critically ill adults: a retrospective cohort study. Intensive Crit Care Nurs. 2020 doi: 10.1016/j.iccn.2020.102924. [DOI] [PubMed] [Google Scholar]
- 27.Edsberg LE, Langemo D, Baharestani MM, Posthauer ME, Goldberg M. Unavoidable pressure injury: state of the science and consensus outcomes. J Wound Ostomy Cont Nurs. 2014;41:313–334. doi: 10.1097/WON.0000000000000050. [DOI] [PubMed] [Google Scholar]
- 28.Manzano F, Perez-Perez AM, Martinez-Ruiz S, et al. Hospital-acquired pressure ulcers and risk of hospital mortality in intensive care patients on mechanical ventilation. J Eval Clin Pract. 2014;20:362–368. doi: 10.1111/jep.12137. [DOI] [PubMed] [Google Scholar]
- 29.Halfens R, Bours G, Ast W. Relevance of the diagnosis ‘stage 1 pressure ulcer’: an empirical study of the clinical course of stage 1 ulcers in acute care and long-term care hospital populations. J Clin Nurs. 2001;10:748–757. doi: 10.1046/j.1365-2702.2001.00544.x. [DOI] [PubMed] [Google Scholar]
- 30.Doerken S, Mandel M, Zingg W, Wolkewitz M. Use of prevalence data to study sepsis incidence and mortality in intensive care units. Lancet Infect Dis. 2018;18(3):252. doi: 10.1016/S1473-3099(18)30081-1. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
Study protocol, statistical analysis plan, and informed consent forms will be shared upon request with any researcher. Local DecubICUs investigators have the right to use the data collected from their respective units. National data can be obtained and used by the DecubICUs National Representatives upon proof of written consent from the local investigators. The complete DecubICUs database is only transferred to the primary investigators, SOL and SIB. They cannot share the database as they are bound to a broad variety of Data User Agreements. Information requests are to be addressed to stijn.blot@ugent.be and sonia.labeau@hogent.be.