Background

At the height of the coronavirus disease 2019 (COVID-19) pandemic, Italy had the highest number of deaths in Europe; most occurred in the Lombardy region. Up to 4% of patients with COVID-19 required admission to an intensive care unit because they developed a critical illness (eg, acute respiratory distress syndrome). Numerous patients with acute respiratory distress syndrome who had been admitted to the intensive care unit required rescue therapy like prone positioning.

Objective

To describe the respiratory management of and the extensive use of prone positioning in patients with COVID-19 at the intensive care unit hub in Lombardy, Italy.

Methods

A total of 89 patients (67% male; median age, 59 years [range, 23-80 years]) with confirmed COVID-19 who were admitted between February 23 and March 31, 2020, were enrolled in this quality improvement project.

Results

Endotracheal intubation was required in 86 patients (97%). Prone positioning was used as rescue therapy in 43 (48%) patients. Significantly more younger patients (age ≤ 59 years) were discharged alive (43 of 48 [90%]) than were older patients (age ≥ 60 years; 26 of 41 [63%]; P < .005). Among the 43 patients treated with prone ventilation, 15 (35% [95% CI, 21%-51%]) died in the intensive care unit, of which 10 (67%; P < .001) were older patients.

Conclusions

Prone positioning is one strategy available for treating acute respiratory distress syndrome in patients with COVID-19. During this pandemic, prone positioning can be used extensively as rescue therapy, per a specific protocol, in intensive care units.

This article has been designated for CE contact hour(s). The evaluation tests your knowledge of the following objectives:

  1. Identify a critically ill patient with respiratory failure who is eligible for prone positioning.

  2. List all clinical activities necessary to prepare the patient before the pronation maneuver.

  3. Demonstrate the correct head and limb positions to prevent the risk of neural tissue injury.

To complete evaluation for CE contact hour(s) for activity C2123, visit www.ccnonline.org and click the “CE Articles” button. No CE fee for AACN members. This activity expires on April 1, 2023.

The American Association of Critical-Care Nurses is accredited as a provider of nursing continuing professional development by the American Nurses Credentialing Center’s Commission on Accreditation, ANCC Provider Number 0012. AACN has been approved as a provider of continuing education in nursing by the California Board of Registered Nursing (CA BRN), CA Provider Number CEP1036, for 1 contact hour.

In December 2019, a series of pneumonia cases emerged in Wuhan, Hubei Province, China.1  The cause of the pneumonia was unknown. Deep sequencing analysis of samples from the patients’ lower respiratory tracts indicated a novel coronavirus, which was named, according to the International Committee on Taxonomy of Viruses, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2).2  The World Health Organization announced on February 11, 2020, that coronavirus disease 2019 (COVID-19) would be the official name of the disease caused by SARS-CoV-2, and 1 month later it declared that COVID-19 had become pandemic.3 

Clinical presentation of COVID-19 ranges from no symptoms to severe pneumonia; the most commonly reported clinical symptom among hospitalized patients is fever, followed by cough, dyspnea, myalgia, and fatigue. Data from the European Centre for Disease Prevention and Control showed that 30% of people diagnosed with COVID-19 were hospitalized, and 4% of those required critical care (as of March 25, 2020).4 

At least 1 health care worker must be an expert in how to perform the prone positioning maneuver.

The first person-to-person transmission in Italy was reported on February 20, 2020, leading to a chain of infections that represents one of the largest COVID-19 out-breaks in Europe to date. Italy, in particular the Lombardy region, has had the largest number of deaths caused by SARS-CoV-2 (11 591 deaths) among countries worldwide and has had the largest number of cases (101 730) in Europe, as of March 31, 2020.5 

Severe lung infection caused by COVID-19 often requires oxygen therapy or noninvasive ventilation to treat severe hypoxemia.6  Most oxygen delivery strategies in spontaneously breathing patients involve risks of aerosolization and disease transmission.7  Use of a helmet to achieve continuous positive airway pressure carries a lower risk of aerosolization than does a high-flow nasal cannula or noninvasive ventilation with a vented mask.8  At the beginning of the pandemic, the best practice for con-trolling the risk of viral aerosolization was to limit the use of noninvasive ventilation and encourage early endotracheal intubation, because late or emergency intubation in rapidly deteriorating patients could be associated with increased risks to patients (because of their poor oxygen reserve) and to health care professionals (because their risk of being exposed to viral load secretions is higher during unplanned procedures).9,10 

Immediately after intubation or transportation to a referral center, patients with COVID-19 presented a pneumonia that, despite meeting most of the Berlin definition criteria for acute respiratory distress syndrome (ARDS),11  is a specific disease with distinctive features such as severe hypoxemia (Pao2-Fio2 ratio < 100) and bilateral pulmonary infiltrates with near-normal respiratory system compliance.12  In this phase of the illness, deep sedation and administration of neuromuscular blocking agents were considered necessary to facilitate mechanical ventilation.13  Lung-protective ventilation is fundamental to clinical management; initial goals must include a tidal volume of less than or equal to 6 to 8 mL/kg per kilogram of predicted body weight, a respiratory rate with target arterial blood pH of 7.30 to 7.42, and regulation of Fio2 to obtain an Spo2 value of about 92% to 95%.14  Several therapeutic options exist for patients with COVID-19 and severe hypoxemia who require endotracheal intubation. One such option is to place the patient in the prone position, which promotes more homogenous aeration of the lungs and improves oxygenation.15  Nursing priorities in the management of patients being placed in the prone position are directed toward optimizing oxygenation and ventilation (including properly positioning the patient, preventing oxygen desaturation, and promoting the clearance of secretions), preventing aspiration events, and maintaining surveillance for complications.

The aim of this quality improvement report is to describe the extensive use of prone positioning as treatment for patients with ARDS and COVID-19 in the intensive care unit (ICU) at Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, a specialized center in Milan, Italy, that was designated as the coordinating hub of ICUs throughout Lombardy, leading the region’s response to the outbreak.16 

Methods

In prone ventilation, ventilation is delivered while the patient lies in the prone position; it is not considered a mode of mechanical ventilation but an advance treatment of severe ARDS that consistently improves oxygenation.17  The main beneficial effects of prone positioning on gas exchange seem to stem from pulmonary recruitment that increases lung volume and reduces the number of atelectatic regions, improved respiratory mechanics, and the facilitation of drainage of secretions.18  Numerous trials have consistently demonstrated the efficacy of prone positioning through improved oxygenation.19-21  One randomized trial and several meta-analyses also suggested that it provides a survival benefit in patients with severe ARDS.22-24 

Patients with COVID-19 and severe ARDS, however, present some different characteristics related to pulmonary recruitment and lung compliance (ie, the measure of the lungs’ ability to stretch and expand).12  For this reason, prone positioning should be considered more as a rescue maneuver that facilitates the redistribution of pulmonary blood flow, rather than a measure for opening collapsed areas, and it should be performed in patients with seriously impaired gas exchange (Pao2-Fio2 ratio < 100) after supine ventilation has been optimized.12  The duration of prone positioning should be 12 to 16 hours per day, and if severe hypoxemia persists while the patient is supine (the position that allows nurses to more easily provide basic nursing care), prone positioning can be immediately reestablished.25 

Prone ventilation of critically ill patients is not without risks (eg, the need for heavier sedation or a higher dose of a neuromuscular blocking agent, hemodynamic instability, device displacement, pressure ulcers), and only experienced and adequately trained personnel should place patients in the prone position.26  Before doing so, health care workers must consider some contraindications (Table 1).18,27  At least 4 health care workers should perform the pronation maneuver.28  Considering the critical condition of patients with COVID-19, however, an additional person—an expert team leader to coordinate preparation and the position change— should also be included to guarantee safety and minimize all possible risks. The incidence of these risks decreases when the team is experienced and when a mattress is used that facilitates the mechanics of safe prone positioning.29  All the procedures described hereafter are performed according to our protocol.

Patients should be placed in the prone position on a pressure-relieving mattress.

Before Prone Positioning

Before starting, make sure that all necessary therapeutic and diagnostic procedures have been performed with the patient in the supine position, as the duration of prone positioning is prolonged.25  To ensure that the maneuver is executed safely, all necessary materials must be prepared in advance and made available to providers. The patient preparation phase includes 3 steps: (1) cleansing the eyes with sterile water solution, administering lubricant gel drops, and closing the eyes with a wound closure strip across the eyelids (eye patches that could compress the orbit and cause edema should not be used)30 ; (2) performing oral hygiene and checking the fixation of the endotracheal tube to guarantee adequate anchorage31,32 ; and (3) assessing the skin’s condition and using hydro-colloid dressings to protect various anatomical points (forehead, cheekbones, thorax, iliac crests, knee) from pressure ulcers.33  It is also important to verify the correct pressure of the endotracheal tube cuff (20-30 cm H2O), aspirate gastric contents, and stop enteral feeding until the end of the maneuver.34  Arterial blood gas values must be analyzed before the maneuver to evaluate gas exchange and the Pao2-Fio2 ratio; these results will establish prospectively the effectiveness of the maneuver with regard to the patient’s oxygenation.

In addition to the organizational and clinical aspects, the patient must be placed on a specific mattress to prevent pressure ulcers. Ideally, all ICU beds should have a pressure-relieving mattress, and all patients who are classified as having a high risk of pressure ulcers should be placed on a low-air-loss mattress upon admission to the ICU. Such a mattress can prevent pressure ulcers from developing on areas such as the face, breasts/chest, genitals, knees, and toes. Patients are typically not at risk for such injury when they are placed supine, but the risk increases when they are in the prone position.35 

During Prone Positioning

Monitoring of oxygen saturation, end-tidal carbon dioxide, and invasive arterial blood pressure is a standard requirement during prone positioning.36  Anterior electrocardiographic electrodes can be removed, provided that they are reattached to the posterior chest at the end of the maneuver. Five health care professionals must be involved: 4 operators position the patient and 1 coordinates and protects the endotracheal tube. While 2 operators ensure the stability and patency of the endotracheal tube, 1 nurse evaluates the arterial and intravenous catheters and other drainage tubes, and 2 other nurses roll the patient using double bedsheets. Both are positioned at 1 side of the bed, and they use the bottom bedsheet to pull the patient toward them, to the edge of the bed. Only when the endotracheal tube and vascular catheters are secured does the team gently roll the patient into the prone position. Head and limb positions are important; their correct positioning prevents the risk of neural tissue injury and the development of limb contractures. The patient should be placed in the “swimmer position,” ensuring that the head is positioned so the face looks toward the ventilator and the limbs are positioned with 1 arm raised at the same side of the face and the other arm alongside the body, thereby preventing abnormal extension or flexion of the shoulders and elbows (Figure 1). The position of both the head and arms should be alternated every 2 to 4 hours.37  The feet should be maintained in dorsiflexion, with the ankle at 90°, and the toes should not touch the rigid structure of the bed.38  Use of a low-air-loss pressure mattress ensures that pressure is reduced and avoids the need to use thoracopelvic supports. In fact, thoracopelvic supports are not recommended because they increase the contact pressure between the supports and the body (thereby nullifying the effect of the pressure-relieving mattress), decrease chest wall compliance, and increase pleural pressure.39  All nonessential monitoring equipment that had been removed before the maneuver must be reattached (ie, electrocardiographic electrodes should be placed on the patient’s posterior chest) and enteral feeding resumed. Complications that occur immediately after placing the patient in the prone position, such as severe hypotension, bradycardia, or prolonged decrease of oxygen saturation (Spo2 < 85%, measured with pulse oximetry), require immediate cessation of prone positioning.

Supination

The supination maneuver is usually simpler than pronation, but it requires the same number of health care workers. One operator ensures the stability of the endotracheal tube and assesses patient positioning during all phases of the procedure, because significant lip, face, and airway edema can develop when a patient is prone. All precautions taken for the pronation maneuver should be followed (eg, aspirate gastric contents and stop enteral feeding, discontinue nonessential infusions, check chest drains if present). While returning a patient to the supine position, nurses align the limbs along the body to avoid joint damage and then turn the patient horizontally, toward the ventilator. Two nurses on the ventilator side pull the rolled-up bedsheets from beneath the patient, while the other 2 nurses (on the opposite side) carefully turn the patient into the supine position. At the end of the maneuver, the team repositions all monitoring equipment that had been removed. If the endotracheal cuff develops a leak, a nurses should immediately recheck the position of the endotracheal tube to ensure that the tube has not moved. For this reason, all appropriate intubation equipment should be immediately available to facilitate effective repositioning/reintubation (should the need for it arise) every time the patient’s position is changed. Hydrocolloid dressings used to prevent pressure ulcers should not be removed if another cycle of prone positioning is planned unless they are dirty or detached.40 

Our ICU created a protocol for all prone positioning procedures. The clinical indications to be evaluated at the patient’s bedside were summarized in a decision-making algorithm to help all health care workers perform a safe procedure (Figure 2).

Results

As of March 31, 2020, a total of 114 640 people had tested positive for SARS-CoV-2 in Lombardy, and 1324 had been admitted to an ICU. All patients who had a laboratory-confirmed SARS-CoV-2 infection and were subsequently admitted to the ICU at Ospedale Maggiore Policlinico between February 23 and March 31, 2020, were enrolled in this quality improvement project. The institutional ethics board at Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico approved the study. We routinely collected clinical data during practice, beginning in the first hours following patients’ ICU admission. Recorded data included age, sex, mode of respiratory support (noninvasive or invasive mechanical ventilation), use of prone positioning and related adverse events, mortality, and ICU discharge. Table 2 shows the demographic and clinical characteristics of the 89 patients admitted during the study period, grouped by age. The median age was 59 (IQR, 49-65; range, 23-80) years; 65 (73%) patients were men (P < .001, exact binomial test), who were similarly distributed among all age groups. To enable comparisons, we split patients into younger (age ≤ 59 years) and older (age ≥ 60 years) groups on the basis of median age.

The correct positioning of head and limbs prevents the risk of neural tissue injury and the development of limb contractures.

Most patients were admitted to the ICU because of acute hypoxemic respiratory failure requiring advanced respiratory support. Endotracheal intubation and mechanical ventilation were required in 86 patients (97%) admitted to the ICU, whereas noninvasive ventilation was used in 2 younger patients and in only 1 older patient; that patient was 80 years old and received ventilation as end-of-life treatment.

Of the 89 patients, 43 (48%) were placed in the prone position as a rescue therapy, for a total of 142 sessions with a median duration of 18 (IQR, 12-21) hours. Prone positioning was used more often in the older group (51%) than in the younger group (46%), but the difference was not statistically significant (P = .67, Fisher exact test). Prone positioning sessions were interrupted 9 times (6%): 5 because of obstruction by pulmonary secretions and oxygen desaturation, 3 because of severe hypotension and hemodynamic instability, and 1 because of tension pneumothorax, which was treated with a chest tube that allowed drainage. Each of these clinical events required the patient to be placed back in the supine position. No unplanned extubation occurred and no chest drainage tube was accidentally removed during any prone positioning maneuver.

A total of 28 pressure ulcers developed in 16 of 43 prone patients (37%) at various anatomical sites: sacral region (n = 6), chin (n = 5), cheekbone (n = 4), heel (n = 4), genitals (n = 2), occiput (n = 2), nasal fold (n = 2), temple (n = 2), and knee (n = 1). Most of these patients (n = 10, 63%) developed pressure ulcers on the frontal surface of the body as a result of prone positioning.

The percentage of patients who were discharged alive from the ICU was higher among younger patients (90% [43 of 48]) than older patients (63% [26 of 41]) (P < .005, Fisher exact test). The overall median length of stay in the ICU was 17 (IQR, 11-37) days. The length of stay of patients who died in the ICU was just 10 (IQR, 6-13) days— shorter than the stays of patients who survived. Mortality in the ICU was 35% (95% CI, 21%-51%) among patients treated with prone ventilation; most of those patients (67%) were older (P < .001, exact binomial test).

Discussion

Among our sample, invasive mechanical ventilation was used much more frequently than indicated by data from the Lombardy region (88%)41  and in a report from Wuhan, China (47%).42  In addition, the percentage of patients who required noninvasive ventilation was low when compared with the 56% reported in another study,43  probably because it is used more often outside the ICU (eg, in specialized wards such as pneumology) and because recommendations made at the beginning of the pandemic suggested limiting the use of noninvasive ventilation to avoid generating viral aerosols, which are associated with a high risk of staff contamination.44  Moreover, during the COVID-19 pandemic, clinicians developed new alternative strategies to avoid intubation, such as the use of the prone position in patients who are awake and can breathe spontaneously while receiving noninvasive ventilation outside the ICU.45  This strategy could become a therapeutic intervention in the future, though patient tolerance is an important limitation of the technique; in addition, the physiological effects of prone positioning have not yet been clarified and the benefits of short sessions are questionable.46 

During the COVID-19 pandemic, Grasselli et al41  reported that 27% of patients (240 of 875) were treated with prone ventilation in all the ICUs of the Lombardy region—a value significantly lower (P < .001, Fisher exact test) than that reported here; our number involves only patients treated in a referral ICU specializing in the management of ARDS. Before the COVID-19 pandemic, at our center, 5 health care workers (4 nurses and 1 physician) usually performed the pronation maneuver in the late afternoon, restoring the patient to the supine position the next morning (according to the patient’s clinical condition) to guarantee that the patient spent enough time in the prone position. This clinical organization allowed our expert staff to safely execute the maneuver and ensured we had an adequate number of staff to do so, particularly as fewer ICU personnel usually work the night shift. During the COVID-19 pandemic, the extensive use of this rescue therapy among critically ill patients has increased the workload for nursing staff and has involved health care workers who may not be experts in this procedure. Staff experience is an important factor in preventing complications. The only randomized controlled trial to show the benefit of prone positioning for patients with severe ARDS was performed by staff with 5 years of experience with prone positioning, and the rate of complications (eg, unplanned extubation, endotracheal tube obstruction, hemoptysis, arterial desaturation, and severe hemodynamic instability) was no different between patients in the prone position and those placed supine.22  The lack of differences in the complications in that study may suggest that ICUs with sufficient experience with managing patients in the prone position could expect a limited number of complications.

Nurses have the primary responsibility for positioning and monitoring patients, so training is essential for them to acquire the necessary skills.

As reported in the literature, we found that the most common adverse effects of prone positioning were pressure ulcers and obstruction by pulmonary secretions, which required an urgent bronchoscopy.24  The risk of developing pressure ulcers is higher among patients in the prone position than among those in the supine position47 ; for this reason, preventive measures must be implemented to protect the anatomical sites that are more at risk. In particular, facial and ocular edema associated with prolonged pressure on the skin increases the risk of ischemic lesions on the face.40  Despite this risk, prone ventilation is a safe procedure, and the overall incidence of recorded adverse events is low (no accidental extubation, tube displacement, or loss of arterial or venous access catheters).

The mortality rate among our patients has been in keeping with rates described in previous reports; such rates differed from 28% to 56% among patients who required ICU admission.48,49  Our mortality rate also confirms that older age is associated with death in patients with COVID-19.

Nurses in the ICU have the primary responsibility for positioning and monitoring patients, so training is essential for them to acquire the necessary skills.50  During the emergency phase of the COVID-19 pandemic, non-ICU staff members supplemented ICU staff to provide sufficient coverage. To facilitate staff integration, our center planned an intensive education program about the most important aspects of nursing care for critically ill patients with SARS-CoV-2 infection, and a period of continuous supervision by senior critical care nurses. Use of protocols, including an algorithmic approach to evaluation, is important to guide those staff members who have less experience in the advanced clinical management of critically ill patients.51 

Limitations

This report has some limitations because of the sample size and the specific use of prone positioning as a rescue therapy during the COVID-19 pandemic. The application of prone positioning only as a rescue therapy for patients with refractory hypoxemia could explain the higher mortality rate among those patients; rescue therapies are only temporary methods that are meant to support or replace respiratory function in patients with severe ARDS who are receiving mechanical ventilation. Finally, this report describes a limited sample from a single center, which could affect the generalizability of these findings.

Conclusion

Prone positioning is 1 strategy, along with mechanical ventilation, that is available to intensive care providers to buy time for patients with ARDS; it allows such patients to maintain pulmonary gas exchange sufficient for survival.52  This aspect is crucial because no specific vaccine or effective treatment yet exists for SARS-CoV-2 infection.53  During the ongoing COVID-19 pandemic, prone positioning can be applied extensively in a hub ICU, and providers should use specific protocols to support decisions and limit the occurrence of complications.

Acknowledgments

The authors thank all the intensive care unit nurses and physicians at Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico for their continuous extraordinary efforts in caring for these critically ill patients.

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Footnotes

To purchase electronic or print reprints, contact the American Association of Critical-Care Nurses, 27071 Aliso Creek Rd, Aliso Viejo, CA 92656. Phone, (800) 899-1712 or (949) 362-2050 (ext 532); fax, (949) 362-2049; email, reprints@aacn.org.

 

Financial Disclosures

None reported.

 

See Also

To learn more about prone positioning, read “Acute Respiratory Distress Syndrome and Prone Positioning” by Mitchell and Seckel in AACN Advanced Critical Care, 2018;29(4):415-425. Available at www.aacnacconline.org.