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Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2021 Oct 29;69:103158. doi: 10.1016/j.iccn.2021.103158

Short and long-term complications due to standard and extended prone position cycles in CoViD-19 patients☆

Alberto Lucchini a,⁎, Vincenzo Russotto b, Nicola Barreca a, Marta Villa a, Giulia Casartelli c, Yelenia Marcolin c, Barbara Zyberi c, Domenico Cavagnuolo c, Giacomo Verzella c, Roberto Rona a, Roberto Fumagalli d, Giuseppe Foti a
PMCID: PMC8554071  PMID: 34895799

Abstract

Objective

To investigate short and long-term complications due to standard (≤24 hours) and extended (>24 hours) prone position in COVID-19 patients.

Methods

Retrospective cohort study conducted in an Italian general intensive care unit. We enrolled patients on invasive mechanical ventilation and treated with prone positioning. We recorded short term complications from the data chart and long-term complications from the scheduled follow-up visit, three months after intensive care discharge.

Results

A total of 96 patients were included in the study. Median time for each prone positioning cycle (302 cycles) was equal to 18 (16–32) hours. In 37 (38%) patients at least one cycle of extended pronation was implemented. Patients with at least one pressure sore due to prone position were 38 (40%). Patients with pressure sores showed a statistically significative difference in intensive care length of stay, mechanical ventilation days, numbers of prone position cycles, total time spent in prone position and the use of extended prone position, compared to patients without pressure sores. All lesions were low grade. Cheekbones (18%) and chin (10%) were the most affected sites. Follow-up visit, scheduled three months after intensive care discharge, was possible in 58 patients. All patients were able to have all 12 muscle groups examined using theMedical Research Council scale examination. No patient reported sensory loss or presence of neuropathic pain for upper limbs.

Conclusions

Extended prone position is feasible and might reduce the workload on healthcare workers without significant increase of major prone position related complications.

Keywords: Brachial Plexus injuries, Extended prone position, Follow-up, Pressure Sores, Prone Position

Implications for clinical practice.

  • •

    Prone positioning requires a nursing protocol to prevent the occurrence of complications.

  • •

    Extended prone positioning is feasible without significant increase of prone position related complications.

  • •

    Extended prone positioning could be suggested in a scenario of a pandemic outbreak to reduce nursing workload.

  • •

    Prone position avoiding “swimmer position” is safe and could help to reduce long term complications on the upper limbs.

Introduction

In patients with Adult Respiratory Distress Syndrome (ARDS), prone positioning (PP) decreased 28-day and 90-day mortality (Guérin et al., 2020). Several studies have shown its impact on gas exchange (Gattinoni et al., 2001, Guérin et al., 2018, Taccone et al., 2009). It is crucial to underline that the improvement of the pO2/FiO2 mmHg ratio value on its own, does not represent the only parameter to evaluate the benefits of prone position. PP, compared to the supine positioning, markedly reduced the overinflated lung areas while promoting alveolar recruitment (Guérin et al., 2013). These effects may contribute to prevent ventilator-induced lung injury by homogenizing the distribution of stress and strain within the lung and they may represent the mechanisms by which PP reduced mortality independently from its effect on oxygenation. COVID-19 pandemic dramatically increased ICU admission of patients with moderate to severe ARDS, leading to the greatest healthcare crisis of the modern era. The sudden lack of intensive care units (ICU) beds, during the first and the second COVID waves, forced healthcare systems to convert hospital areas to new COVID-19 ICUs (Bambi et al., 2020, Grasselli et al., 2020, Lucchini et al., 2020b). This was accompanied by the recruitment of healthcare workers without previous critical care experience. At a time of uncertain efficacy of the available therapies, PP represented the single intervention with proven efficacy for mortality reduction of COVID-19 related ARDS (Nasa et al., 2021). During the pandemic, in Italy, PP has been adopted in 61% of the COVID-19 ICU population (Langer et al., 2021). Despite PP is a well recognized routine intervention for ARDS patients, with a low incidence of short and long term adverse events, PP sessions may be highly demanding for the whole ICU staff considering the high global workload and limited resources. Prone positioning increases the risk of developing hospital-acquired pressure injury (González-Seguel et al., 2021, Sud et al., 2014). The main preventive strategies to prevent pressure sores development during prone positioning include skin assessment (before, during and after PP), repositioning to offload pressure points on the face and the body, application of dressings, such as hydrocolloids, transparent film and silicone, to decrease facial skin breakdown (National Pressure Injury Advisory Panel, 2019). Many ICUs have updated their protocols for pressure sores prevention in PP patients, reflecting necessary changes related to care for COVID-19 patients (Team et al., 2021b). Johnson et al. (2021) recently reported that having a certified wound and skin care nurse on a multi-professional prone-positioning team could help to reduce odds of pressure injuries developing in patients infected with COVID-19. Development of online learning resources (infographics, learning modules and webinars) and a dedicated check-list for PP procedure (Santos et al., 2021) are recently reported to improve and disseminate knowledge about prevention of PP complications (Team et al., 2021a). Preventive strategies recommended by the guidelines suggest to avoid extended use of prone positioning unless required for the management of the individual’s medical condition. (National Pressure Injury Advisory Panel, 2019). However, COVID-19 ARDS management requires prone positioning for extended periods of time (Nasa et al., 2021). A preliminary report of COVID-19 patients proposed the use of prolonged PP (i.e. 36 hours) to improve oxygenation and to reduce nursing workload (Carsetti et al., 2020). The investigators reported that prolonged PP was feasible and safe. The strategy of prolonged pronation cycles may theoretically be of benefit during the low resources of the pandemic by reducing the overall number of daily handling while offering this intervention to the highest number of patients as feasible for a longer time-interval. On the other hand, this intervention may theoretically be associated with a higher risk of pressure sores, facial oedema or peripheral nerve injuries. To our knowledge, these short and long-term consequences of extended pronation cycles have not been systematically investigated to date. Given the growing number of centers adopting this strategy of extended pronation cycles, it would be relevant to collect information on its advantages and shortcomings for a risk–benefit balance. We designed a retrospective cohort study in order to assess safety of extended pronation cycles in COVID-19 ARDS patients, with a specific focus on pressure sores and peripheral nerve injuries assessed at a 3-month follow-up. The secondary aim was to investigate the modifications of the PaO2/FiO2 mmHg ratio induced by prone position.

Materials and methods

Study design

This was a retrospective cohort study conducted between February 2020 and January 2021 in the general ICU of San Gerardo University Hospital, Monza, Italy. The ICU consisted of 10 beds before COVID-19 outbreak. During first wave (February-May 2020) ICU beds increased to 21, while in the second wave (October 20-January 21) the beds increased to 19.

Inclusion and exclusion criteria

We enrolled all consecutive patients with a diagnosis of COVID-19 pneumonia, under invasive mechanical ventilation and prone position. Indication for PP was placed in patients with moderate to severe ARDS and PaO2/FiO2 ratio < 150 mmHg and FiO2 > 0.6. Every prone position cycle was planned for a minimum of 16 hours according to Guerin et al. (Guérin et al., 2013, Foti et al., 2020, Nasa et al., 2021). However, some patients were maintained prone for more than 24 hours to reduce nursing workload (Rezoagli et al., 2021). We classified as “Standard pronation” every PP cycle lasting ≤ 24 hours, and as “extended pronation” every PP cycle > 24 hours. We registered all complications related to PP applications (i.e. displacement of indwelling catheters, facial oedema, pressure sores, vomiting, unplanned extubation, airway obstruction due to bronchial secretion retention with need of unplanned bronchoscopy and haemodynamic instability) (Lucchini et al., 2020a). The National Pressure Ulcer Advisory Panel (NPUAP) score was used to classify the pressure sores (Edsberg et al., 2016). The Braden Score was used for predicting pressure ulcer risk. We also calculated the PaO2/FiO2 ratio, at the following time-points: before pronation (PRE-supine step), one hour after pronation (1 h-PP step), at the end of pronation (END-PP step) and one hour after supination (POST-supine step).

Prone position ICU protocol

Every prone positioning manoeuvre was performed according to our ICU protocol and policy, which is described in detail in Supplementary material _S1 (Bein et al., 2015; Bruni et al., 2020; Lucchini et al., 2017; Lucchini et al., 2020a). Prone position protocol includes the need to protect bony prominences with prophylactic dressing prior to prone positioning, lubricate the eyes and tape them closed, ensure that the endotracheal tube be secured with tapes (National Pressure Injury Advisory Panel, 2019). Our ICU policy, from January 2020 avoided implementation of “swimming position”. Fig. 1 showed a patient in prone position. Supplementary material Fig. S2 showed the pillows used in the study period.

Fig. 1.

Fig. 1

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Patient in prone position with transversal rolls.

Follow-up visit

We followed up COVID-19 patients three months after ICU discharge. In order to detect neuromuscular injuries as long term complications of PP, we extracted Follow-Up reports on the assessment of muscle peripheral strength by the Medical Research Council (MRC) scale and hand-held dynamometry (Council, 1976, Hermans et al., 2012, Parry et al., 2015). The MRC Scale for muscle strength is a commonly used scale for assessing muscle strength from Grade 5 (normal) to Grade 0 (no visible contraction). This score was defined as the sum of MRC scores from six muscles in the upper and lower limbs on both sides, so that the score ranged from 60 (normal) to 0 (quadriplegic). Handgrip strength dynamometry has been proposed as a simple and easy diagnostic method for ICU acquired weakness and was performed on both upper limbs (Bragança et al., 2019, Van Aerde et al., 2020).

Ethical issue

Data were collected as part of the “STORM” study (Spallanzani Institute approval number 84/2020; NCT04424992).

Statistical analysis

We performed the D’Agostino-Pearson test to assess the normal distribution of variables. Variables with normal distribution were reported as mean and standard deviation (SD) and comparison between their means was performed using the Student’s t test. Variables without a normal distribution were reported as median and interquartile range (IQR) and comparison between two groups was performed using the Mann-Whitney U test. Categorical data are reported as frequencies (%) and their difference tested by Chi-Square’s or Fisher’s exact test as appropriate. One-way repeated measures analysis of variance (rmANOVA) were used to evaluate the differences at the different time points (PRE-supine step: before pronation, 1 h – PP step: one hour after pronation, END-PP Step: at the end of pronation, POST-supine step: one hour after resupination) of the PO2/FiO2 ratio values and respiratory parameters. A p value < 0.05 was considered statistically significant. All data were analysed using the Statistical Social Sciences software, version 22.0, for Macintosh (SPSS Inc., Chicago, IL, USA).

Results

Prone position results during ICU stay

From February 20, 2020 to January 31, 2021, 108 patients were admitted to our ICU with a confirmed diagnosis of COVID-19. A total of 96 patients were included in the study. The median age was 59 years (IQR: 53–66), 22 (23%) were female and the median ICU length of stay was 15 days (7–25). At ICU admission patients presented a median Braden score of 10 (10–11) with a median Body Mass Index of 28 (26–33). Comorbidities included hypertension (52% - n = 19), type 2 diabetes mellitus (23%, n = 17%) and arteriopathies (10% - n = 7). Median pO2/FiO2 before the first PP cycle was 116 (82–148), while the median time in hours, from ICU admission to first PP manoeuvre was equal to 8 (4–45) hours. Median time for each PP performed cycle was equal to 18 (16–32) hours. PP was applied for one cycle in 30 (31%) patients, for two cycles in 21 (22%), for three cycles in 16 (17%), while patients who received three or more PP cycles were 29 (30%). In 37 (38%) patients at least one cycle of extended pronation was implemented. The overall time for patients, spent in PP was equal to 48 (31–101) hours. In 13 (13%) subjects PP was adopted while the patient was connected to veno-venous Extracorporeal Membrane Oxygenation. 79 (82%) patients survived and were discharged from ICU.

Pronation-related adverse events

Patients with at least one pressure sore due to PP were 38 (40%). Patients with pressure sores showed a statistically significative difference in ICU length of stay, mechanical ventilation days, numbers of PP cycles, total time spent in PP and the use of extended prone position, compared to patients without pressure ulcers. Chin and cheekbones were the most affected sites, where pressure sores were present in 18% (n = 17) and 10% (n = 10%) of patients. Regarding the pressure ulcer severity, the most frequent stage of NPUAP score was stage II in 93 out of 105 pressure sores (88%), followed by stage I in 9 pressure sores (8.5%) and stage III in 3 sites (3.5%). No pressure sores with stage IV occurred. The characteristics of the sample, and the difference between patients without and with pressure sore development are presented in Table 1 . Incidence of medical device-related pressure injuries in mucosal tissues, because of prone positioning, such as ulcers of the lips were present in 7 patients (7%) caused by endotracheal tubes, but we did not record pressure sores in ala nasi and nostrils due to nasogastric tubes.

Table 1.

Descriptive characteristics of enrolled patients. with and without pressure sores.

All patientsn=96
(100%)		 Patients without Pressure Sores related to PP n=58 (60%) Patients with Pressure Sores related to PP n=38 (40%) p.value
Sex Female n= (%) 22 (23%) 15 (26%) 7 (18%) 0.396
Age (years) - Median (IQR) 59 (53-67) 60 (54-68) 59 (51-66) 0.463
Lenght of ICU stay (days) 15 (7-25) 15 (6-21) 19.5 (10-28) 0.038
Weight - cm - Median (IQR) 80 (75-95) 80 (75-95) 82. 5 (80-95) 0.762
BMI - Median (IQR) 28 (26 -33) 28 (26-33) 28 (26-33) 0.784
<24.9 - normal weight 20 (21%) 12 (21%) 8 (21%) 0.961
24.9 -29.9 - overweight 39 (41%) 24 (42%) 15 (40%)
>30.0 obesity 36 (38%) 21 (37%) 15 (40%)
Diabetes - yes 17 (23%) 8 (18%) 9 (30%) 0.216
Hypertension - yes 39 (52%) 26 (56%) 13 (43%) 0.22
Arteriopathies- yes 7 (10%) 4 (10%) 3 (12%) 0.79
Alive at ICU discharge - n=(%) 79 (82%) 51 (88%) 28 (74%) 0.074
Median Braden (ICU admission day) 10 (10-11) 10 (10-10) 10 (9-11) 0.899
ARDS classification mild 4 (4%) 3 (5%) 1 (3%)
moderate 53 (55%) 35 (60%) 18 (47%) 0.299
severe 39 (41%) 20 (35%) 19 (50%)
median PO2/FiO2 ratio (first PP manouvre) 116 (82-148) 121 (86-150) 98 (69-145) 0.095
Mechanical ventilation days 13 (7-20) 12 (5-18) 15 (10-23) 0.033
Veno-Venous ECMO - yes 13 (13%) 5 (9%) 8 (21%) 0.082
Tracheostomy -yes 21 (22%) 14 (24%) 7 (18%) 0.508
Norepinephrine infusion during PP cycles - yes 57 (60%) 34 (60%) 23 (61%) 0.205
Dopamine infusion during PP cycles 26 (27%) 19 (33%) 7 (18%) 0.631
Median Time from admission to first PP- hours 8 (4-45) 7.5 (4-36) 12 (5-48) 0.324
Median Time for each PP cycle - hours 18 (16-32) 17 (15-32) 21(16-32) 0.053
Median Prone Position cycle per patient 2 (1- 4) 2 (1-4) 3 (2-4) 0.017
1 cycle 30 (31%) 26 (45%) 4 (10%) 0.336
2 cycles 21 (22%) 10 (17%) 11 (29%)
3 cycles 16 (17%) 6 (105) 10 (26%)
> 3 cycles 29 (30%) 16 (28%) 13 (35%)
Total time in Prone Position - hours 48 (31-101) 38 (20-84) 65 (34-126) 0.005
Extended Prone Postion - yes 37 (38%) 18 (31%) 19 (50%) 0.062
PP cycle - Median Highest Time - hours 41 (29-43) 41 (37-42) 41 (40-44) 0.327
Pressure sores at ICU Admission - yes 3 (3%) 0 (0%) 3 (8%) 0.03
Number of body areas with pressure sores at ICU admission 2 (2-2) 0 2 (2-2) 0.074
Pressure sores at ICU discharge - yes 56 (59%) 18 (32%) 38 (100%) <0.0001
Number of body areas with pressure sores at ICU discharge 2 (1-3) 1 (1-2) 2 (1-3) 0.0721
Pressure sores related to Prone Position
Median number of body areas with Pressure sores related to PP 1 (1 -2) --- 1 (1-2) ---
Forehead 4 (4%) --- 4 (10%)
Forehead - median NPUAP grade 2 (2-2) --- 2 (2-2)
Cheekbones 10 (10%) --- 10 (26%)
Cheekbones - median NPUAP grade 2 (2-2) --- 2 (2-2)
Chin 17 (18%) --- 17 (44%)
Chin - median NPUAP grade 2 (2-2) --- 2 (2-2)
Lips 7 (7%) --- 7 (18%)
Lips - median NPUAP grade 2 (2-2) --- 2 (2-2)
Thorax 9 (9%) --- 9 (24%) 1
Thorax - Median NPUAP grade 2 81-2) --- 2 (1-2)
Abdomen 1 (1%) --- 1 (3%)
Abdomen - median NPUAP grade 2 --- 2
Iliac crests 3 (3%) --- 3 (8%)
Iliac crests - median NPUAP grade 2 (2-2) --- 2 (2-2)
Tibial plateau 3 (3%) --- 3 (8%)
Tibial plateau - median NPUAP grade 2 (2-2) --- 2 (2-2)
Knees 9 (9%) --- 9 (24%) 1
Knees - median NPUAP grade 2 (2-2) --- 2 (2-2)
Other sites with Pressure sores 4 (4%) --- 4 (11%)
Other sites - median NPUAP grade 2 (2-2) --- 2 (2-2)
Pressure sores not related to Prone Position
Occiput 1 (1%) --- 1 0.214
Occiput - NPUAP grade 2 --- 2
Shoulder blades 14 (15%) 11 (19%) 3 (8%) 0.133
Shoulder blades - median NPUAP grade 2 (2-2) 2 (2-2) 2 (2-2)
Sacrum 23 (24%) 9 (16%) 14 (37%) 0.017
Sacrum - median NPUAP grade 2 (2-2) 2 (2-3) 2 (2-2)
Buttocks 2 (2%) 2 (3%) --- 0.247
Buttocks - median NPUAP grade 2 (1-2) 2 (1-2) ---
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PP: Prone Position. BMI : Boby Mass Index. ARDS : adult respiratory distress syndrome. ECMO : extracorporeal membrane oxygenation. NPUAP : National Pressure Ulcer Advisory Panel.

Extended PP was implemented in 37 (39%) of enrolled patients. Patients undergoing extended pronation had a median of 34 (30–41) hours versus 16 (15–18) (p < 0.0001) of patient receiving standard pronation, a higher total time spent in PP [85(43–136) versus 33 (18–64) hours – p < 0.0001] during ICU stay, a higher number of proning cycles [3 (2–4) versus 2 (1–4) – p = 0.017]. The prevalence of patients with pressure sore was 51% (n = 19) for patient with extended pronation and 32% (n = 19) in patient with standard pronation (p = 0.032). Difference between patients undergoing standard versus extended pronation are presented in Table 2 .

Table 2.

Descriptive characteristics of patients undergone standard versus extended pronation.

Patients without extended prone position
n=59 (61%)		 Patients with extended prone positionn=37
(39%)		 p.value
Sex Female - n= (%) 15 (26%) 7 (20%) 0.461
Age (years) - Median (IQR) 60.0 (53.0-68.0) 58.0 (55.0-66.0) 0.851
Lenght of ICU stay (days) 15.0 (7.0-20.0) 20.0 (11.0-28.0) 0.039
Weight cm - Median (IQR) 85.0 (75.0-96.0) 80.0 (80.0-90.0) 0.256
BMI - Median (IQR) 27.7 (26-32.7) 27.75 (25.7 - 32.9) 0.161
Alive, n=(%)   48 (81%) 31 (84%) 0.762
Median PO2/FiO2 ratio (first Prone Position manouvre) 120 (86-150) 111 (71 -145) 0.328
Mechanical ventilation days 13 (6-18) 15 (10-24) 0.096
Veno-Venous ECMO - yes 6 (10%) 7 (19%) 0.223
Tracheostomy - yes 12 (20%) 9 (24%) 0.646
Median Time from admission to first prone position - hours 8 (4-60) 6 (4-41) 0.281
Median Time for each prone position cycle - hours 16 (15–18) 34.0 (30-41) 0.0001
Median Prone Position cycle per patient 2 (1-4) 3 (2-4) 0.017
Total time in Prone Position - hours 33 (18-64) 85 (43-136) 0.0001
Highest Cycle Time in extended prone position- hours 41 (39-43) 0.327
Median Braden score (ICU admission day) 10 (9 -10) 10 (10 -11)
   
Pressure sores due to prone position 19 (32%) 19 (51%) 0.032
Number of body areas with Pressure sores related to PP 1 (1-1) 2 (1-3) 0.042
Forehead 1 (2%) 3 (8%) 0.126
Forehead - median NPUAP grade 2 (2–2) 2 (2-2) 1.000
Cheekbones 6 (10%) 4 (10%) 0.920
Cheekbones - median NPUAP grade 2 (2–2) 2 (2-2) 0.662
Chin 8 (14%) 9 (24%) 0.179
Chin - median NPUAP grade (2–2) 2 (2-2) 0.481
Lips 3 (5%) 4 (11%) 0.294
Lips - median NPUAP grade 2 (2-2) 2 (2-3) 0.629
Thorax 3 (5%) 6 (16%) 0.069
Thorax - Median NPUAP grade 2 (1-2) 2 (2-2) 0.517
Abdomen 0 (0%) 1 (3%) 0.204
Abdomen - median NPUAP grade --- 2 ---
Iliac crests 2 (3%) 1 (3%) 0.851
Iliac crests - median NPUAP grade 2 (2-2) 2 (2-2) 1.000
Tibial plateau 0 (0%) 3 (9%) 0.026
Tibial plateau - median NPUAP grade --- 2 (2-2) ----
Knees 1 (2%) 6 (16%) 0.069
Knees - median NPUAP grade 1 (1-2) 2 (2-2) 0.117
Other sites with Pressure sores 1 (1%) 3 (8%) 0.126
Other sites - median NPUAP grade 2 (2-2) 2 (2-2) 0.988
Pressure sores not related to Prone Position
Occiput 0 (0%) 1 (3%) 0.204
Occiput - NPUAP grade --- 2 -----
Shoulder blades 11 (19%) 3 (8%) 0.155
Shoulder blades - median NPUAP grade 2 (2-2) 2 (2-2) 0.458
Sacrum 16 (27%) 7 (19%) 0.360
Sacrum - median NPUAP grade 2 (2-3) 2 (2-2) 0.671
Buttocks 1 (2%) 1 (3%) 0.737
Buttocks - median NPUAP grade 2 1 0.987
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ECMO: extracorporeal membrane oxygenation, NPUAP : National Pressure Ulcer Advisory Panel.

The total pronation manoeuvres investigated were 302. Extended pronation was most commonly used during the second COVID-19 wave. The overall complications related to PP manoeuvre were haemodynamic instability in 29 (10%) manoeuvres, prolonged arterial desaturation involved 57 (19%) of investigated cycles and bronchial secretions retention, with need of unplanned bronchoscopy, occurred in 33 (11%) manoeuvres. No accidental removal of vascular access devices occurred during the study period, while we observed 2 (1%) nasogastric tube and one (0.5%) endotracheal tube displacement, with no necessity to device repositioning (no completely extubation was occurred). No statistically significant differences in these severe complications were detected between standard and extended pronation cycles. Details about all investigated prone position cycles and related complications are reported in Table 3 . PO2/FiO2 ratio improved during prone position and after resupination compared to baseline (i.e. before prone position) in overall cycles and in extended versus standard pronation groups, as showed in Fig. 2 . Table S3 (see Additional file 3) summarizes all mechanical ventilation and oxygenation data.

Table 3.

Description of prone positioning cycles and complications

All cyclesn=302
(100%)		 Standard pronationn=227
(75%)		 Extended pronationn=75
(25%)		 p.Value
COVID-19 Wave first 144 (48%) 143 (63%) 1 (2%) <0.0001
second 158 (52%) 84 (37%) 74 (98%)
Veno-Venous ECMO (yes) 36 (16%) 30 (16%) 6 (14%) 0.734
Norepinefrine infusion – (yes) 120 (48%) 91 (51%) 29 (39%) 0.077
Norepinephrine dosage (mcg/Kg/min) 0.06 (0.04-0.07) 0.06 (0.04-0.08) 0.04 (0.03-0.07) 0.007
Dopamine infusion – (yes) 53 (23%) 42 (26%) 11 (16%) 0.088
Dopamine dosage (mcg/Kg/min) 4.1 (2.35 - 5.19) 4.1 (2.3-5.26) 3.07 (2.42-5.00)  0.080
Medical device displacement Endotracheal tube n= (%) 1 (0.5%) 1 (0.5%) 0 (0%) 0.565
Nasogastric Tube n= (%) 2 (1%) 2 (1%) 0 (0%) 0.455
Vascular catheters n=(%) 0 (0%) 0 (0%) 0 (0%) ---
Hemodynamic instability - n=(%) 29 (10%) 22 (10%) 7 (9%) 0.927
Prolonged Arterial Desaturation - n=(%) 57 (19%) 45 (20%) 12 (16%) 0.463
Bronchial secretions retention - n=(%) 33 (11%) 26 (12%) 7 (9%) 0.610
Vomit – n=(%) 0 (100%) 0 (0%) 0 (0%) ---
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Fig. 2.

Fig. 2

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pO2/FiO2 ratio in the investigated time steps: before pronation (PRE-supine step), one hour after pronation (1h-PP step), at the end of pronation (END-PP step) and one hour after supination (POST-supine step).

Three months follow up visit

Follow Up visit, three months after ICU discharge, by anaesthesiologist and ICU nurse was possible in 58 patients. In the remaining 36, the main reasons for the missed visit were: distance from the hospital (patient centralized during COVID and referred to the local hospital) and refusal to visit. No patient reported problems with pressure sores outcomes at the three-month follow-up visit. All patients were able to have all 12 muscle groups examined by MRC examination. Median overall MRC score at Follow Up visit was 60 (59–60). We did not observe significantly difference in MRC score in patients undergoing standard prone position compared to patients with extended pronation [60 (59–60)] versus 60 (58–60) -p = 0.395]. For the following tested districts: shoulder adductors, elbow flexors and wrist extensor, the MRC score was always ≥3 in all patients. Foot dorsiflexors test was equal to zero in one patient (left side) and in two patients was equal to one (right side). We observed one patient with grade zero in MRC score in left foot dorsiflexors test. Hip flexors test was grade two in one patient (right side). Statistically significance was reported in MRC grade distribution, between patients with and without extended pronation only for the right Elbow flexors test (p = 0.028). Table 4 summarize results from MRC all 12 muscle groups examined. After physical examination, no patient reported sensory loss or presence of neuropathic pain for upper limbs. The median overall maximum handgrip dynamometry was 33.0 (24–37) kg-force. Finally, we did not observe any difference between standard and extended pronation groups in handgrip dynamometry results [33(25.0–37) vs. 29 (20–39) kg-force - p = 0.679].

Table 4.

MRC Test results in patients undergoing three months follow-up visit.

Muscle Side MRC Scale
Grade 0 Grade 1 Grade 2 Grade 3 Grade 4 Grade 5
Shoulder adductors Left 0 (0%) 0 (0%) 0 (0%) 1 (2%) 12 (21%) 45 (78%)
Right 0 (0%) 0 (0%) 0 (0%) 2 (3%) 8 (14%) 48 (83%)
Elbow flexors Left 0 (0%) 0 (0%) 0 (0%) 0 (0%) 8 (14%) 50 (86%)
Right 0 (0%) 0 (0%) 0 (0%) 1 (2%) 6 (10%) 51 (88%)
Wrist extensor Left 0 (0%) 0 (0%) 0 (0%) 0 (0%) 7 (12%) 51 (88%)
Right 0 (0%) 0 (0%) 0 (0%) 1 (2%) 6 (10%) 51 (88%)
Hip flexors Left 0 (0%) 0 (0%) 0 (0%) 0 (0%) 9 (16%) 49 (84%)
Right 0 (0%) 0 (0%) 1 (2%) 0 (0%) 8 (14%) 49 (84%)
Knee extensors Left 0 (0%) 0 (0%) 0 (0%) 0 (0%) 9 (16%) 49 (84%)
Right 0 (0%) 0 (0%) 0 (0%) 0 (0%) 8 (14%) 50 (86%)
Foot dorsiflexors Left 1 (2%) 0 (0%) 0 (0%) 1 (2%) 9 (16%) 47 (81%)
Right 0 (0%) 2 (3%) 0 (0%) 1 (2%) 8 (14%) 47 (81%)
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Grade 5: Normal, Grade 4: Movement against gravity and resistance, Grade 3: Movement against gravity over (almost) the full range, Grade 2: Movement of the limb but not against gravity, Grade 1: Visible contraction without movement of the limb (not existent for hip flexion), Grade 0: No visible contraction.

Discussion

Prone position for ventilated patients with COVID-19 ARDS was strongly suggested by experts, for a duration of 16–24 hours per session, similar to the indication in non-COVID-19-related ARDS (Nasa et al., 2021). In our study the rate of pressure sores was similar to the results of the studies published before the Covid-era (Lucchini et al., 2018a, Lucchini et al., 2020a, Sud et al., 2014), but lower if we consider recent studies on PP and COVID-19 patients (Binda et al., 2021, Douglas et al., 2021, Ibarra et al., 2020). Binda and colleagues, in a retrospective study in a single ICU in Italy, involved 63 COVID-19 patients with a total of 219 proning cycles, report an incidence of prone-related pressure ulcers in about 30% of patients (Binda et al., 2021). Ibarra and colleagues, in Spain, published a case-series of patients on invasive mechanical ventilation and PP therapy with 77% of the patients presented pressure sores due to PP (Ibarra et al., 2020). The frequency of pressure sores in the face area, found in our study was lower than those reported in two systematic reviews (Abroug et al., 2008, Sud et al., 2014) and in a narrative review (González-Seguel et al., 2021) in which pressure ulcers occurred in 34%, 43% and 19% of patients, respectively. Important to underline that we didn’t detected grade III in the reported pressure sores developed on face area. Low-grade facial pressure sores have less serious consequences, and none of our patients needed special care or treatment. All the pressure sores were managed with dressings, achieving wound healing by secondary intention in all the survivors (Perrillat et al., 2020, Shearer et al., 2021). Once their condition improved and prone positioning was no longer performed, the skin fully recovered in all patients. No patient reported any problems with pressure sore outcomes at the follow-up visit, after ICU discharge.

Comparing the incidence of pressure sores with two studies published by our group (Lucchini et al., 2018a, Lucchini et al., 2020a) in the last 5 years, however, we must note that the global incidence has slightly increased. In our previously study on PP complications, ICU team was composed only by ICU nurses with long experience in nursing and management of ARDS patients. During the COVID-era, human and material health care resources had to be adapted to an unpredictable new “war” scenario in a very short period of time (Bambi et al., 2020, Lucchini et al., 2020b, Lucchini et al., 2020c). In a few days, the growing demand for COVID-19 patients ICU beds in our region, forced us, during the first wave (February-April 20) to realise 11 new beds in the operating theatre in addition to our 10 bed ECMO unit. The original ICU staff were divided between the new and the old ICU beds. 33 nurses from the operating theatre were also recruited as new ICU staff. In this context, it is understandable that the complications of this procedure could increase. In order to guarantee a safe PP procedure, at least three experienced operators (critical care nurses and/or Intensivist physicians) were present during each prone position manoeuvre. During second wave only 10 nurses from the operating theatre were recruited. Even for this shortage of nurses, the use of extended prone position became frequent in our ICU, during the second pandemic wave (Rezoagli et al., 2021). In addition to the reduced nurses’ experience, the nurse-to-patient ratio changed between the first and second COVID-19 waves. In the first wave there was always, a nurse-to patient ratio equal to 1: 2. In the second wave, the nurse-to-patient ratio of 1:2 was always guaranteed only for ECMO patients. In the other patients, the nurse-to-patient ratio was 1:2.5.

Patients undergoing “extended prone position” in our study, trended to a higher number of proning cycles [3 (2–4) versus 2 (1–4) - p = 0.017] and to a longer time spent in prone position during their ICU stay compared to standard PP group [33 (18–64) versus 85 (43–136), p = 0.0001]. Oxygenation improvement in our sample seemed to be higher during “extended pronation” than during standard pronation, and after resupination compared to baseline. The risk of developing a higher incidence of pressure sores in the prolonged extended pronation is an issue that should be cautiously monitored in present and future studies (National Pressure Injury Advisory Panel, 2019). In our sample we observed an increased rate of pressure sores (51% extended PP vs. 32% standard PP – p = 0.0001), but we did not observe an increase of the others PP complications.

In previously published metanalyses and narrative reviews (Abroug et al., 2008, González-Seguel et al., 2021, Sud et al., 2014 ;) the total percentage of airway related complications described for prone position were present in a range between 20 and 40% of investigated cycles. We did not observe any unplanned extubation. In all patients, our ICU policy provided that the artificial airway was secured with a 5 cm canvas tape placed upon a thin hydrocolloid (Lucchini et al., 2018b). Before every pronation, the tape was replaced in order to guarantee better stability (National Pressure Injury Advisory Panel, 2019). Moreover, before pronation, the tube was displaced on the side of the mouth not leaning on the pillow (for example when the head was rotated on the right side, the tube was fixed on the right, and vice versa). Our protocol included the use of thin hydrocolloid as protective skin coverings, under devices and over bony prominences (forehead, cheeks, chin, iliac crest, ribs and patella and tibial plateau) (Lucchini et al., 2020a, Peko et al., 2020). The regular use of hydrocolloids, may be a beneficial factor in decreasing skin breakdown in PP (National Pressure Injury Advisory Panel, 2019). The current evidence suggests that positioning devices to offload pressure points on the face and body are a useful addition within an overall PU prevention strategy (Binda et al., 2021, Peko et al., 2020, Rodríguez-Huerta et al., 2021).

Finally, no long term adverse events due to PP have been observed during the follow-up visit. Nerve injuries are uncommon following prone positioning (Goettler et al., 2002), but brachial plexus injuries have been recently reported (Brugliera et al., 2021, Douglas et al., 2021, Miller et al., 2021). Brachial plexus injuries could occur in PP patients when shoulders are positioned in abduction with external rotation and posteriorly displaced and this position causes compression and stretching of the brachial plexus, usually affecting the upper nerve roots (Bozentka, 1998). Recently Miller et al. (2021), in a study involving 256 COVID-19 patients with PP, reported that in 12 (5%) patients the ulnar nerve was injured, and in 11 patients, an injury was presents at the cords of the brachial plexus. 30 (10%) patients reported neuropathic pain, and all patients presented with motor weakness. Brugliera et al, (2021) reported 7 (5%) cases of brachial plexopathy out of 135 patients who had undergone in PP, in an Italian ICU. Douglas et al. (2021) reported brachial plexus palsies in five (8.2%) of 61 patients treated with extended pronation. In all these studies, the ICU teams used a standard protocol for PP, with implementation of the “swimming position”, always combined with alternating arm reposition, performed between 2 or 4 h. Generally, authors that reported the “swimming position” adoption, are unable to extract exactly data on the frequency of arm cycling while patients were proned. The “swimming position” involves raising one arm on the same side to which the head is facing while placing the other arm by the patient’s side. The shoulder should be abducted to 80 degrees and the elbow flexed 90 degrees on the raised arm. This is, however, a potential stretch position for the ulnar nerve at the elbow (Bozentka, 1998). Before the study period, the prone position protocol in our unit involved the use of the “swimming position”. In this position, our protocol before December 2019, required that only the left arm was raised (Lucchini et al., 2018a, Lucchini et al., 2020a). In an internal audit (December 2019) we reported two cases of brachial plexus injury detected at the scheduled follow-up visit. For this reason, in order to investigate the possible rule of “swimming position” in those adverse events developments, we decided, starting from January 2020, avoid it during PP. Shortly after this decision, the COVID-era began in Italy and in our ICU (Giani et al., 2020, Lucchini et al., 2020b). All enrolled patients in our study were pronated by keeping the limbs along the body and avoiding programmed repositioning. The upper limbs were positioned trying to avoid shoulders abduction and external rotation or posteriorly displacing and to avoid elbow flexion positions. For the lower limbs, we maintained a slight flexion of the knees, trying to avoid the extra rotation of the feet.

MRC scale carried out during the three-month visit after discharge from the ICU showed the absence of complications related to the upper limbs in the investigated patients. Our results are encouraging, albeit not definitive. Future multicentric studies on the role of “swimming position” and frequency of arm cycling, on peripheral nerve injuries development could provide increased insights and help to design new guideline for prone position. The consequences of upper limb peripheral nerve injuries are potentially life changing and devastating for ICU survivors.

Limitations

Several limitations should be considered in the interpretation and generalization of these findings. First, one limitation may be considered the single-centre, retrospective design. Second, data on complications were recorded in a pandemic period characterized by a reduction in the usual nurse-patient ratio, and an increased workload with a potential for underestimation of pressure sores detection. However, this is the first study which primarily investigated and reported the most expected complications from prolonged pronation cycles. Third, follow-up visit was possible only in 58 patients and we cannot exclude the presence of complications in patients missed to follow-up.

Conclusions

This retrospective study has shown that, even during a pandemic surge, coupled with limited resources, prone position could be applied with an acceptable increase in complications rate. Extended prone positioning is feasible although with a slight increase in the incidence of low severity pressure sores respect to standard prone position and no major serious complications have been reported. Extended prone positioning could be currently suggested in a scenario of a pandemic outbreak. Prone position protocol should include the need to protect bony prominences with prophylactic dressing, lubricate the eyes and tape them closed and endotracheal tube securing only with tapes, repositioning to offload pressure points on the face and the body and use of positioning devices. Prone position avoiding “swimmer position” is safe and could help to reduce long term complications on the upper limbs. Preventive measures of potential complications of prone positioning, including airway obstruction, pressure injuries, and brachial plexopathies, should be implemented in intensive care settings whenever possible, even during a pandemic period. Monitoring of prone position long term complications should be part of the follow-up programs for ICU survivors. Future research in prevention of short and long term complication should address at least the following four issues: 1) impact of “swimmer position” on upper limb peripheral nerve injuries on a large population, 2) role of different positioning devices (viscoelastic versus polystyrene balls or polyurethane, 3) identification of the best prophylactic dressing (hydrocolloids, transparent film, and silicone) to decrease facial skin breakdown, 4) impact on gas exchange and mortality of extended pronation cycles.

Financial support

None.

Author contributions

AL, VR, MV, RR, RF and GF conception and design of the study, manuscript writing and final approval. NB, MV, GC, YM, BZ, DC, GV : data collection. AL, MV, NB GC, YM.: statistical analysis. All authors have read and approved the final manuscript.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Footnotes

☆

The present study was performed at the General Intensive Care Unit, Emergency Department and Intensive Care, San Gerardo Hospital – ASST Monza, Via Pergolesi 33 – Monza (MB), Milan-Bicocca University – Italy.

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.iccn.2021.103158.

Appendix A. Supplementary data

The following are the Supplementary data to this article:

Supplementary Fig. S1.

Supplementary Fig. S1

Open in a new tab

Devices and pillows used in the study period. 1 Transversal rolls, 2 and 3 Face cushion, 4 Pillow for hands and arms – pillows with polystyrene microspheres, Askle medical – France, 5 Mölnlycke® Z-Flo™ Adult Fluidized Positioner 64 x 91 cm, 6 Mölnlycke® Z-Flo™ Adult Fluidized Positioner 41 × 76 cm.

Supplementary data 1
mmc1.docx (25KB, docx)
Supplementary data 2
mmc2.docx (14KB, docx)

References

  1. Abroug F., Ouanes-Besbes L., Elatrous S., Brochard L. The effect of prone positioning in acute respiratory distress syndrome or acute lung injury: a meta-analysis: areas of uncertainty and recommendations for research. Intensive Care Med. 2008;34:1002–1011. doi: 10.1007/s00134-008-1062-3. [DOI] [PubMed] [Google Scholar]
  2. Bambi S., Iozzo P., Lucchini A. New issues in nursing management during the COVID-19 pandemic in Italy. Am. J. Crit. Care. 2020;29:e92–e93. doi: 10.4037/ajcc2020937. [DOI] [PubMed] [Google Scholar]
  3. Bein T.h., Bischoff M., Brückner U., Gebhardt K., Henzler D., Hermes C., Lewandowski K., Max M., Nothacker M., Staudinger T.h., Tryba M., Weber-Carstens S., Wrigge H. S2e guideline: positioning and early mobilisation in prophylaxis or therapy of pulmonary disorders : Revision 2015: S2e guideline of the German Society of Anaesthesiology and Intensive Care Medicine (DGAI) Anaesthesist. 2015;64(S1):1–26. doi: 10.1007/s00101-015-0071-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Binda F., Galazzi A., Marelli F., Gambazza S., Villa L., Vinci E., Adamini I., Laquintana D. Complications of prone positioning in patients with COVID-19: a cross-sectional study. Intensive Crit. Care Nurs. 2021;67:103088. doi: 10.1016/j.iccn.2021.103088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bozentka D. Cubital tunnel syndrome pathophysiology: clinical orthopaedics and related research®. Clin. Orthop. Relat. 1998;351:90–94. [PubMed] [Google Scholar]
  6. Bragança R.D., Ravetti C.G., Barreto L., Ataíde T.B.L.S., Carneiro R.M., Teixeira A.L., Nobre V. Use of handgrip dynamometry for diagnosis and prognosis assessment of intensive care unit acquired weakness: a prospective study. Heart Lung. 2019;48(6):532–537. doi: 10.1016/j.hrtlng.2019.07.001. [DOI] [PubMed] [Google Scholar]
  7. Brugliera L., Filippi M., Del Carro U., Butera C., Bianchi F., Castellazzi P., Cimino P., Capodaglio P., Monti G., Mortini P., Pradotto L.G., Priano L., Spina A., Iannaccone S. Nerve compression injuries after prolonged prone position ventilation in patients with SARS-CoV-2: a case series. Arch. Phys. Med. Rehabil. 2021;102(3):359–362. doi: 10.1016/j.apmr.2020.10.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bruni A., Garofalo E., Grande L., Auletta G., Cubello D., Greco M., Lombardo N., Garieri P., Papaleo A., Doldo P., Spagnuolo R., Longhini F. Nursing issues in enteral nutrition during prone position in critically ill patients: a systematic review of the literature. Intensive Crit. Care Nurs. 2020;60:102899. doi: 10.1016/j.iccn.2020.102899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Carsetti A., Damia Paciarini A., Marini B., Pantanetti S., Adrario E., Donati A. Prolonged prone position ventilation for SARS-CoV-2 patients is feasible and effective. Crit. Care. 2020;24:225. doi: 10.1186/s13054-020-02956-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Council M.R. Her Majesty’s Stationary Office; London: 1976. Aids to the Investigation of Peripheral Nerve Injuries. [Google Scholar]
  11. Douglas, I.S., Rosenthal, C.A., Swanson, D.D., Hiller, T., Oakes, J., Bach, J., et al., 2021.Safety and outcomes of prolonged usual care prone position mechanical ventilation to treat acute Coronavirus Disease 2019 hypoxemic respiratory failure. Crit. Care Med. 49, 490–502. doi: 10.1097/CCM.0000000000004818. [DOI] [PubMed]
  12. Edsberg L.E., Black J.M., Goldberg M., McNichol L., Moore L., Sieggreen M. Revised national pressure ulcer advisory panel 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]
  13. Gattinoni L., Tognoni G., Pesenti A., Taccone P., Mascheroni D., Labarta V., Malacrida R., Di Giulio P., Fumagalli R., Pelosi P., Brazzi L., Latini R. Effect of prone positioning on the survival of patients with acuterespiratory failure. N. Engl. J. Med. 2001;345(8):568–573. doi: 10.1056/NEJMoa010043. [DOI] [PubMed] [Google Scholar]
  14. Giani M., Seminati D., Lucchini A., Foti G., Pagni F. Exuberant plasmocytosis in bronchoalveolar lavage specimen of the first patient requiring extracorporeal membrane oxygenation for SARS-CoV-2 in Europe. J. Thorac Oncol. 2020;15:65–e66. doi: 10.1016/j.jtho.2020.03.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. González-Seguel F., Pinto-Concha J.J., Aranis N., Leppe J. Adverse events of prone positioning in mechanically ventilated adults with acute respiratory distress syndrome. Respir Care. 2021;respcare.09194 doi: 10.4187/respcare.09194. [DOI] [PubMed] [Google Scholar]
  16. Goettler C.E., Pryor J.P., Reilly P.M. Brachial plexopathy after prone positioning. Crit. Care. 2002;6:540–542. doi: 10.1186/cc1823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Grasselli G., Pesenti A., Cecconi M. Critical care utilization for the COVID-19 outbreak in Lombardy, Italy: early experience and forecast during an emergency response. JAMA. 2020;323:1545–1546. doi: 10.1001/jama.2020.4031. [DOI] [PubMed] [Google Scholar]
  18. Guérin C., Reignier J., Richard J.-C., Beuret P., Gacouin A., Boulain T., Mercier E., Badet M., Mercat A., Baudin O., Clavel M., Chatellier D., Jaber S., Rosselli S., Mancebo J., Sirodot M., Hilbert G., Bengler C., Richecoeur J., Gainnier M., Bayle F., Bourdin G., Leray V., Girard R., Baboi L., Ayzac L. Prone positioning in severe acute respiratory distress syndrome. N. Engl. J. Med. 2013;368(23):2159–2168. doi: 10.1056/NEJMoa1214103. [DOI] [PubMed] [Google Scholar]
  19. Guérin C., Beuret P., Constantin J.M., Bellani G., Garcia-Olivares P., Roca O., Meertens J.H., Maia P.A., Becher T., Peterson J., Larsson A., Gurjar M., Hajjej Z., Kovari F., Assiri A.H., Mainas E., Hasan M.S., Morocho-Tutillo D.R., Baboi L., Chrétien J.M., François G., Ayzac L., Chen L., Brochard L., Mercat A. A prospective international observational prevalence study on pronepositioning of ARDS patients: the APRONET (ARDS Prone Position Network)study. Intensive Care Med. 2018;44(1):22–37. doi: 10.1007/s00134-017-4996-5. [DOI] [PubMed] [Google Scholar]
  20. Guérin C., Albert R.K., Beitler J., Gattinoni L., Jaber S., Marini J.J., Munshi L., Papazian L., Pesenti A., Vieillard-Baron A., Mancebo J. Prone position in ARDS patients: why, when, how and for whom. Intensive Care Med. 2020;46(12):2385–2396. doi: 10.1007/s00134-020-06306-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Foti G., Giannini A., Bottino N., Castelli G.P., Cecconi M., Grasselli G., Guatteri L., Latronico N., Langer T., Monti G., Muttini S., Pesenti A., Radrizzani D., Ranucci M., Russotto V., Fumagalli R. Management of critically ill patients with COVID-19: suggestions and instructions from the coordination of intensive care units of Lombardy. Minerva Anestesiol. 2020;86(11) doi: 10.23736/S0375-9393.20.14762-X. [DOI] [PubMed] [Google Scholar]
  22. Hermans G., Clerckx B., Vanhullebusch T., Segers J., Vanpee G., Robbeets C., Casaer M.P., Wouters P., Gosselink R., Van Den Berghe G. Interobserver agreement of Medical Research Council sum-score and handgrip strength in the intensive care unit. Muscle Nerve. 2012;45(1):18–25. doi: 10.1002/mus.v45.110.1002/mus.22219. [DOI] [PubMed] [Google Scholar]
  23. Johnson, C., Giordano, NA., Patel, L., Book, KA., Mac, J., Viscomi J., et al. 2021. Pressure Injury Outcomes of a Prone-Positioning Protocol in Patients With COVID and ARDS. Am. J. Crit. Care. 2021 Sep 13:e1-e8. doi: 10.4037/ajcc2022242. [DOI] [PubMed]
  24. Ibarra G., Rivera A., Fernandez-Ibarburu B., Lorca-García C., Garcia-Ruano A. Prone position pressure sores in the COVID-19 pandemic: the Madrid experience. J. Plast. Reconstr. Aesthet. Surg. 2020 doi: 10.1016/j.bjps.2020.12.057S1748-6815(20)30732-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Langer T., Brioni M., Guzzardella A., Carlesso E., Cabrini L., Castelli G., Dalla Corte F., De Robertis E., Favarato M., Forastieri A., Forlini C., Girardis M., Grieco D.L., Mirabella L., Noseda V., Previtali P., Protti A., Rona R., Tardini F., Tonetti T., Zannoni F., Antonelli M., Foti G., Ranieri M., Pesenti A., Fumagalli R., Grasselli G. Prone position in intubated, mechanically ventilated patients with COVID-19: a multi-centric study of more than 1000 patients. Crit. Care. 2021;25(1) doi: 10.1186/s13054-021-03552-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lucchini A., Bonetti I., Borrelli G., Calabrese N., Volpe S., Gariboldi R., et al. Enteral nutrition during prone positioning in mechanically ventilated patients. Assist Inferm Ric. 2017;36:76–83. doi: 10.1702/2721.27752. [DOI] [PubMed] [Google Scholar]
  27. Lucchini A., De Felippis C., Pelucchi G., Grasselli G., Patroniti N., Castagna L., Foti G., Pesenti A., Fumagalli R. Application of prone position in hypoxaemic patients supported by veno-venous ECMO. Intensive Crit. Care Nurs. 2018;48:61–68. doi: 10.1016/j.iccn.2018.04.002. [DOI] [PubMed] [Google Scholar]
  28. Lucchini A., Bambi S., Galazzi A., Elli S., Negrini C., Vaccino S., et al. Unplanned extubations in general intensive care unit: A nine-year retrospective analysis. Acta Biomed. 2018;89:25–31. doi: 10.23750/abm.v89i7-S.7815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lucchini A., Bambi S., Mattiussi E., Elli S., Villa L., Bondi H., Rona R., Fumagalli R., Foti G. Prone position in acute respiratory distress syndrome patients: a retrospective analysis of complications. Dimens. Crit. Care Nurs. 2020;39(1):39–46. doi: 10.1097/DCC.0000000000000393. [DOI] [PubMed] [Google Scholar]
  30. Lucchini A., Giani M., Elli S., Villa S., Rona R., Foti G. Nursing Activities Score is increased in COVID-19 patients. Intensive Crit. Care Nurs. 2020;59:102876. doi: 10.1016/j.iccn.2020.102876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lucchini A., Iozzo P., Bambi S. Nursing workload in the COVID-19 era. Intensive Crit. Care Nurs. 2020;61:02929. doi: 10.1016/j.iccn.2020.102929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Miller C., O'Sullivan J., Jeffrey J., Power D. Brachial plexus neuropathies during the COVID-19 pandemic: a retrospective case series of 15 patients in critical care. Phys. Ther. 2021;101:pzaa191. doi: 10.1093/ptj/pzaa191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nasa P., Azoulay E., Khanna A.K., Jain R., Gupta S., Javeri Y., et al. Expert consensus statements for the management of COVID-19-related acute respiratory failure using a Delphi method. Crit. Care. 2021;25(1) doi: 10.1186/s13054-021-03491-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. National Pressure Injury Advisory Panel, European Pressure Ulcer Advisory Panel, and Pan Pacific Pressure Injury Alliance. Prevention and treatment of pressure ulcers/injuries: Clinical practice guideline. Emily Haesler ed. 2019. Osborne Park, Australia: Cambridge Media.
  35. Parry S.M., Berney S., Granger C.L., Dunlop D.L., Murphy L., El-Ansary D., et al. A new two-tier strength assessmen tapproach to the diagnosis of weakness in intensive care: an observational study. CritCare. 2015;19:52. doi: 10.1186/s13054-015-0780-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Peko L., Barakat‐Johnson M., Gefen A. Protecting prone positioned patients from facial pressure ulcers using prophylactic dressings: a timely biomechanical analysis in the context of the COVID-19 pandemic. Int. Wound J. 2020;17(6):1595–1606. doi: 10.1111/iwj.v17.610.1111/iwj.13435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Perrillat A., Foletti J.-M., Lacagne A.-S., Guyot L., Graillon N. Facial pressure ulcers in COVID-19 patients undergoing prone positioning: how to prevent an underestimated epidemic? J. Stomatol. Oral Maxillofac. Surg. 2020;121:442–444. doi: 10.1016/j.jormas.2020.06.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rezoagli E., Mariani I., Rona R., Foti G., Bellani G. Difference between prolonged versus standard duration of prone position in COVID-19 patients: a retrospective study. Minerva Anestesiol. 2021 doi: 10.23736/S0375-9393.21.15864-X. [DOI] [PubMed] [Google Scholar]
  39. Rodríguez-Huerta, M.D., Díez-Fernández, A., Rodríguez-Alonso, M.J., Robles-González, M., Martín-Rodríguez, M., González-García, A. 2021. Nursing care and prevalence of adverse events in prone position: characteristics of mechanically ventilated patients with severe SARS-CoV-2 pulmonary infection. Nurs. Crit. Care. doi: 10.1111/nicc.12606. [DOI] [PMC free article] [PubMed]
  40. Santos V.B., Aprile D.C.B., Lopes C.T., Lopes J.L., Gamba M.A., Costa K.A.L., et al. COVID-19 patients in prone position: validation of instructional materials for pressure injury prevention. Rev. Bras. Enferm. 2021;74(Suppl 1) doi: 10.1590/0034-7167-2020-1185. [DOI] [PubMed] [Google Scholar]
  41. Shearer S.C., Parsa K.M., Newark A., Peesay T., Walsh A.R., Fernandez S., et al. Facial pressure injuries from prone positioning in the COVID-19 era. Laryngoscope. 2021 doi: 10.1002/lary.29374. [DOI] [PubMed] [Google Scholar]
  42. Sud S., Friedrich J.O., Adhikari N.K.J., Taccone P., Mancebo J., Polli F., Latini R., Pesenti A., Curley M.A.Q., Fernandez R., Chan M.-C., Beuret P., Voggenreiter G., Sud M., Tognoni G., Gattinoni L., Guérin C. Effect of prone positioning during mechanical ventilation on mortality among patients with acute respiratory distress syndrome: a systematic review and meta-analysis. CMAJ. 2014;186(10):E381–E390. doi: 10.1503/cmaj.140081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Taccone P., Pesenti A., Latini R., Polli F., Vagginelli F., Mietto C., et al. Prone positioning in patients with moderate and severe acute respiratory distress syndrome. JAMA. 2009;302(18):1977. doi: 10.1001/jama.2009.1614. [DOI] [PubMed] [Google Scholar]
  44. Team V., Team L., Jones A., Teede H., Weller C.D. Pressure injury prevention in COVID-19 patients with acute respiratory distress syndrome. Front. Med. 2021;7 doi: 10.3389/fmed.2020.558696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. V. Team, A., Jones, C.D., 2021b. Weller, Prevention of hospital-acquired pressure injury in COVID-19 patients in prone position, Intensive Crit Care Nurs. Advance online publication. doi: 10.1016/j.iccn.2021.103142. [DOI] [PMC free article] [PubMed]
  46. Van Aerde N., Meersseman P., Debaveye Y., Wilmer A., Gunst J., Casaer M.P., Bruyninckx F., Wouters P.J., Gosselink R., Van den Berghe G., Hermans G. Five-year impact of ICU-acquired neuromuscular complications: a prospective, observational study. Intensive Care Med. 2020;46(6):1184–1193. doi: 10.1007/s00134-020-05927-5. [DOI] [PubMed] [Google Scholar]

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