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      Prone Positioning of Nonintubated Patients with COVID-19

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          To the Editor: Epidemiological data on severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and the disease it causes, coronavirus disease (COVID-19), are quickly emerging. As the pandemic progresses, scarce resources (e.g., ICU beds and mechanical ventilators) may become a rate-limiting factor in the care for these patients. Therefore, therapies to prevent the need for intubation and mechanical ventilation are desperately needed. A recent study describing the respiratory physiology of mechanically ventilated patients with COVID-19–associated acute respiratory distress syndrome (ARDS) showed low respiratory system compliance in the supine position; however, prone positioning increased lung recruitment and improved oxygenation (1). Given the physiological benefits of prone positioning, we hypothesized that patients with COVID-19 and respiratory distress, not yet intubated but at high risk for intubation, might benefit from prone positioning. We conducted a retrospective review of our experience proning a clinical series of nonintubated patients. Methods Patients Between March 23, 2020, and April 15, 2020, nine adult patients at an academic medical center with confirmed positive PCR testing results for SARS-CoV-2 RNA, with rapidly increasing oxygen requirements necessitating ICU admission but not yet requiring intubation, were determined to be appropriate clinical candidates for proning. One additional patient on the medical floor, who required an ICU consult because of increased work of breathing, was also included. Patients requiring urgent mechanical intubation were not eligible for proning. Proning Patients were asked to alternate every 2 hours between a prone and supine position during the day and sleep in a prone position at night, as tolerated. A physician provider supervised the first episode of proning. Patients were asked to self-prone, and nursing staff reminded patients. Outcome measures Primary outcome measures were the change in oxygen saturations and respiratory rate before proning and approximately 1 hour after initial proning compared with preproning. The secondary outcome was the incidence of intubation within 2 weeks of the first prone-positioning trial. All patients were followed for 28 days for hospital discharge status. Outcomes were collected retrospectively via chart review. The retrospective data for this case series were determined to be exempt by the institutional review board at the Johns Hopkins University School of Medicine. Results Three of the 10 patients (30%) were female, and the median age was 56 years (range, 40–80 yr). Before prone positioning, the median oxygen requirement was 40%, with four patients requiring high-flow nasal cannula (HFNC) and five patients requiring nasal cannula. The median time from onset of symptoms to ICU consultation/admission was 8.5 days (range, 5–11 d), and median time from ICU admission to prone positioning was 5 hours (interquartile range [IQR], 2.25–13.25 h). All patients received empirical antimicrobial therapy for possible community-acquired pneumonia. One patient was enrolled in a randomized clinical trial of remdesivir or placebo. Eight patients had bilateral lower-lobe infiltrate on chest imaging, two with an alveolar pattern, three with an interstitial pattern, and three with a mixed alveolar and interstitial pattern. Oxygenation rapidly improved after prone positioning, and at 1 hour after assuming a prone position, median oxygen saturations had increased from 94% (IQR, 91–95%) to 98% (IQR, 97–99%) (Figure 1). Interestingly, after prone positioning, work of breathing had improved, as evidenced by a reduced median respiratory rate from 31 (IQR, 28–39) to 22 (IQR, 18–25) breaths/min (Figure 2). There were no adverse events with prone positioning. Patients endorsed improved dyspnea with prone positioning. Seven of the 10 patients did not require escalation of respiratory care. Eight of the 10 patients did not require intubation. The two patients who required intubation were intubated ∼24 hours after the initial prone positioning. In addition, these two patients also had the highest respiratory support on admission to the ICU, with an Fi O2 of 0.50 and 0.60 on HFNC. At 28 days of follow-up, all patients had been discharged from the hospital to their homes. Figure 1. Oxygen saturations before prone positioning and 1 hour after prone positioning of individual patients. Solid symbols represent patients that required intubation. The P value was determined by using the Wilcoxon matched-pairs signed rank test. LNC = liters of nasal cannula; RA = room air; yoF = year-old female; yoM = year-old male. Figure 2. Respiratory rate before prone positioning and 1 hour after prone positioning of individual patients. Solid symbols represent patients who required intubation. The P value was determined by using the Wilcoxon matched-pairs signed rank test. Discussion Although the value of prone positioning in mechanically ventilated patients with moderate-to-severe ARDS is compelling (2), less is known about the effects of prone positioning in spontaneously breathing, nonintubated adult patients. Case reports and retrospective reviews have demonstrated safety and improvements in oxygenation with prone positioning in patients with ARDS (3–5). In nonintubated patients with COVID-19, prone positioning together with a combined strategy of HFNC and restrictive fluid (6) or noninvasive ventilation (7) improved oxygenation. The effects of prone positioning, without positive pressure ventilation, were not isolated. In this case series, all patients experienced significant improvement in respiratory status during the initial prone-positioning period. Five of the 6 patients on nasal cannula or room air did not require escalation of respiratory care, and 8 of 10 patients did not require invasive mechanical ventilation. The potential mechanism of benefit of prone positioning in nonintubated patients is unlikely to be related solely to improved oxygenation, as past studies have not associated improved oxygenation with survival in ARDS. Homogenous lung aeration with prone positioning (8) could result in reduced respiratory effort and lead to a lower incidence of intubation. Although the data presented herein are intriguing, many questions remain. How long does the effect of proning last? Does the beneficial effect of proning continue after supination? Does proning prevent the need for intubation or merely delay it? Could prone positioning accelerate recovery? There are several limitations in the data from this case series. First, as is common with case series, selection bias is possible. Second, there was no control intervention, and the study sample was small. Third, it is uncertain whether these patients would have improved without prone positioning, although the rapid change, within 1 hour, after proning is suggestive of a favorable impact. Fourth, measures of patient dyspnea or comfort after prone positioning were not collected. Fifth, to minimize the documentation burden on nursing-staff workflow, data on patient adherence to the prone-positioning recommendation beyond the first episode of proning were not collected. Given the potential of prone positioning as a low-cost, easily implemented, and scalable intervention, particularly in low- and middle-income countries, expeditious yet thorough testing of prone positioning in patients at risk for intubation is warranted (e.g., W. Al-Hazzani and colleagues, unpublished results [clinicaltrials.gov identifier NCT 04350723], among others).

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          Lower mortality of COVID-19 by early recognition and intervention: experience from Jiangsu Province

          A cluster of patients of novel coronavirus pneumonia (NCP) have been identified in Wuhan in December 2019 and soon this virus spread at a tremendous rate which swept through the whole China and more than 93 countries and regions around the world [1, 2]. This emerging, rapidly evolving situation has threatened the health of all mankind and WHO has raised COVID-19 risk to “very high” at global level. Up to now, 80,859 cases were confirmed, among which 10–15% patients were critically ill and 3100 (3.83%) died in China. The large number of transmission population between Jiangsu and Hubei provinces led to the infinite burden in controlling the COVID-19 epidemic in Jiangsu Province [3, 4]. By 24:00 on March 7, a total of 631 confirmed cases of NCP were reported with a portion of critically ill patients whose ages ranged from 9 months to 96 years old. A total of 610 cases have been discharged from hospital, and the cure rate of confirmed cases in our province has reached 96.67%, which is far exceeding that of national data [5–8]. Since the outcome of NCP patients in Jiangsu was much better than that in Hubei where the mortality of NCP patients was nearly 4.34%, we retrospectively summarized our therapeutic process and figured out that critical care-dominated treatment patterns might be the core in reducing mortality. Early recognition of high-risk and critically ill patients Since the severity of disease is closely related to the prognosis, the basic and essential strategies to improve outcomes that we should adhere to remain the early detection of high-risk and critically ill patients [9, 10]. During the clinical work in Jiangsu Province, critical care was shifted forward and early screening was measured. All NCP patients were screened twice every day and respiratory rate (RR), heart rate (HR), SpO2 (room air) were monitored regularly. Once SpO2   30/min, HR > 120/min or any signs of organ failure were observed, patients would be transferred to intensive care unit (ICU) and ICU physicians and nurses would take over their treatment. From our data of more than 600 NCP patients in Jiangsu Province, age, lymphocyte count, oxygen supplementation and aggressive pulmonary radiographic infiltrations are independent risk factors for NCP progressing to a critical condition. We established an early warning system combining these four factors to identify high-risk patients and then kept them under continuous close monitoring. The sensitivity of this warning system was 0.955 (95% CI [0.772–0.999]), the specificity was 0.899 (95% CI [0.863–0.928]) and the area under ROC curve was 0.962 (data unpublished). Our retrospective analysis of cases in Jiangsu Province proved a good consistency between early screening of SpO2, RR, HR and early warning model. Therefore, a flowchart integrating early warning model and early screening procedure is recommended for high-risk patients recognition and all patients’ screening to make it possible for early intervention (Fig. 1). Fig. 1 Early warning system and screening procedures for NCP patients Early intervention guided by intensivists Since there have been no effective antiviral treatments for COVID-19 [7, 8], the vital way to reduce mortality is early and strong intervention to prevent the progression of disease. During the treatment of Jiangsu NCP patients, three points which showed valid evidence in reversing the disease and preventing tracheal intubation rate were summarized. (1) For patients with ARDS or pulmonary extensive effusion in CT scan, high-flow nasal cannula oxygen therapy (HFNC) or non-invasive mechanical ventilation (NIV) was used to maintain positive end expiratory pressure (PEEP) to prevent alveolar collapse even if some of these patients did not have refractory hypoxemia. (2) Restrictive fluid resuscitation under the premise of adequate tissue perfusion is performed to relieve pulmonary edema. (3) Although previous study proved prone position’s benefit in moderate-to-severe ARDS patients with invasive mechanical ventilation (IMV) [11], we attempted awake prone position in NCP patients which showed significant effects in improving oxygenation and pulmonary heterogeneity (Fig. 2). With all these measurements, although the rate of critically ill patients in Jiangsu had reached 10%, the IMV rate of Jiangsu was kept under 1%, which was significantly lower than our previous survey about ARDS patients [12]. Fig. 2 Early intervention for patients with critical condition Clinical experts-guided hierarchical management strategy At the outset of epidemic situation, a clinical experts-guided, multidisciplinary, province-wide hierarchical management group was established to provide medical guidance for all NCP patients [13]. The members of this panel are mainly critical care specialists and respiratory specialists from tertiary hospitals. Jiangsu Province is divided into five regions according to geographical position and each leader takes responsibilities for a specific region so that problems can be solved layer-by-layer. This kind of regional responsibility, timely feedback communication management makes it possible for effective medical interventions (Fig. 3). Fig. 3 Organization chart of hierarchical management strategy Rational allocation of materials and human resources Health authorities attached great importance to epidemic and deployed disease prevention and control measures effectively [14, 15]. All kinds of resources, including frontline medical staff and medical protective materials, were mobilized and deployed uniformly to guarantee patients’ medical care. 234 clinical staff invested in NCP patients’ treatment and care, and 3500 clinical staff were reserved for unexpected needs. Adequate material and human resources are important cornerstones for controlling this epidemic. Since the outbreak of COVID-19, Jiangsu takes effective measures to curb the spread of the virus and gives normative treatments for infected patients, which shows significant disease control and treatment effects. From our experience, early screening of critically ill patients and critical care-guided early intervention are prominent in reducing NCP patients’ mortality. At this critical moment in the global outbreak of NCP, we hope our valid management and treatment bundles can help us achieve the victory in the battle against COVID-19.
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            Prone position in acute respiratory distress syndrome. Rationale, indications, and limits.

            In the prone position, computed tomography scan densities redistribute from dorsal to ventral as the dorsal region tends to reexpand while the ventral zone tends to collapse. Although gravitational influence is similar in both positions, dorsal recruitment usually prevails over ventral derecruitment, because of the need for the lung and its confining chest wall to conform to the same volume. The final result of proning is that the overall lung inflation is more homogeneous from dorsal to ventral than in the supine position, with more homogeneously distributed stress and strain. As the distribution of perfusion remains nearly constant in both postures, proning usually improves oxygenation. Animal experiments clearly show that prone positioning delays or prevents ventilation-induced lung injury, likely due in large part to more homogeneously distributed stress and strain. Over the last 15 years, five major trials have been conducted to compare the prone and supine positions in acute respiratory distress syndrome, regarding survival advantage. The sequence of trials enrolled patients who were progressively more hypoxemic; exposure to the prone position was extended from 8 to 17 hours/day, and lung-protective ventilation was more rigorously applied. Single-patient and meta-analyses drawing from the four major trials showed significant survival benefit in patients with PaO2/FiO2 lower than 100. The latest PROSEVA (Proning Severe ARDS Patients) trial confirmed these benefits in a formal randomized study. The bulk of data indicates that in severe acute respiratory distress syndrome, carefully performed prone positioning offers an absolute survival advantage of 10-17%, making this intervention highly recommended in this specific population subset.
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              Lung Recruitability in COVID-19–associated Acute Respiratory Distress Syndrome: A Single-Center Observational Study

              To the Editor: The coronavirus disease (COVID-19) outbreak was declared a public health emergency by the World Health Organization on January 30, 2020. A majority (67–85%) of critically ill patients who were admitted to an ICU with a confirmed infection of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) developed acute respiratory distress syndrome (ARDS) (1, 2). An observational study of 52 cases at a single center, the Jinyintan Hospital (a temporary designated center for critically ill patients with COVID-19) in Wuhan, China, showed that these patients had a high mortality (61.5%) (2). For patients with ARDS, the specific characteristics of this syndrome, such as the respiratory mechanics, remain unknown. In particular, an important clinical question with regard to personalizing the management of these patients is whether the lungs are recruitable with high positive end-expiratory pressure (PEEP) for each individual patient. Two of the authors of this study (C.P. and H.Q.) were directly in charge of these critically ill patients with SARS-CoV-2–associated ARDS at the Jinyintan Hospital. Clinical decisions about the right PEEP level were challenging, especially when the PEEP was adapted based on the NIH-NHLBI ARDS Network PEEP-Fi O2 table. With high PEEP (e.g., 15 cm H2O), the plateau pressure often became extremely high (>45 cm H2O) and patients seemed poorly responsive, often displaying only modest improvement in oxygenation, with increased driving pressure and/or development of hypotension. Because of the high clinical workload and the very constrained environment, these bedside observations were not done in a systematic manner or recorded. Until recently, quantitative assessments of a patient’s potential for lung recruitment at the bedside were very imprecise (3). Recently, members of our group (including L.C., M.C.S., and L.B.) described a new mechanics-based index to directly quantify the potential for lung recruitment, called the recruitment-to-inflation ratio (R/I ratio) (4). It estimates how much of an increase in end-expiratory lung volume induced by PEEP is distributed between the recruited lung (recruitment) and the inflation and/or hyperinflation of the “baby lung” when a higher PEEP is applied. It ranges from 0 to 2.0, and the higher the R/I ratio, the higher the potential for lung recruitment. An R/I ratio of 1.0 suggests a high likelihood of recruitment, as the volume will be distributed similarly to the recruited lung and the baby lung. This method can be performed at the bedside and requires only a single-breath maneuver on any ventilator. This maneuver is particularly useful in conditions of high risk of virus transmission by disconnection, transport, or complex procedures. The clinicians in Wuhan decided to use this measure of recruitment in a systematic way in a series of patients with SARS-CoV-2–associated ARDS, and also to assess the effect of body positioning. Methods This was a retrospective, observational study conducted in a 35-bed ICU at Wuhan Jinyintan Hospital. The institutional ethics review board approved this study (KY-2020-10.02). Written informed consent was waived owing to the observational design of the study and the urgent need to collect data for this infectious disease. The clinical charts of adult patients with laboratory-confirmed COVID-19 admitted to the ICU were reviewed. The patients received invasive mechanical ventilation and met the criteria for ARDS (Berlin definition) (5), were under continuous infusion of sedatives, and were assessed for respiratory mechanics, including lung recruitability, during the week of February 18, 2020. This week (a 6-d observational window) was selected in order for the clinical team to record these additional measurements in the chart. Patients were ventilated in volume-controlled mode with Vt at 6 ml/kg of predicted body weight. Prone positioning was performed over periods of 24 hours when PaO2 /Fi O2 was persistently lower than 150 mm Hg. Flow, volume, and airway pressure were measured by ventilators (SV300; Mindray). Circuit leakage was excluded through a 6-second end-inspiratory occlusion. Measurements were performed at clinically set PEEP levels and were repeated every morning during the observation days, when possible. Total PEEP and plateau pressure were measured by a short end-expiratory and an end-inspiratory occlusion, respectively. Complete airway closure was assessed by performing a low-flow (6 L/min) inflation and by comparing patients' compliance with circuit compliance as previously described (6). The potential for lung recruitment was assessed by means of the R/I ratio (4), which can be calculated automatically from a webpage (https://crec.coemv.ca). Because of the limited access to computers or the internet while under airborne precautions, one of the authors (L.C.) provided a compact form for calculating the R/I ratio manually. In patients without airway closure, R/I ratio = V T e H → L − V T e H V T i × Pplat L − PEEP L PEEP H − PEEP L − 1 where VteH→L indicates the Vt exhaled from high to low PEEP during the single-breath maneuver, VteH is the exhaled Vt at high PEEP, Vti is the preset inspiratory Vt, PplatL is the plateau pressure at low PEEP, and PEEP h and PEEP l denote high and low PEEP, respectively. In patients with airway closure, the low PEEP was replaced with the measured airway opening pressure when the airways were reopened above the airway closure (6). A threshold of 0.5 was used to define high recruitability (R/I ratio ≥ 0.5) and low recruitability (R/I ratio  115 27 23 17 Yes No Alive 9 5 4 9 0.55 128 70 22 12 30 Yes No Alive 10 4 8 12 1.0 90 69 35 25 9 Yes Yes Alive 11 2 1 3 1.0 57 49 35 25 18 Yes Yes Alive 12 7 9 16 1.0 68 58 38 30 14 Yes Yes Alive Mean 4 4 9 0.7 128 66 30 22 20 — — — SD 3 6 6 0.21 53 13 8 9 8 — — — Total — — — — — — — — — 7Y/5N 3Y/9N 9A/3D Definition of abbreviations: ARF = acute respiratory failure; Crs = respiratory system compliance; ∆P = driving pressure; ECMO = extracorporeal membrane oxygenation; IMV =invasive mechanical ventilation; NHF = nasal high flow; NIV = noninvasive ventilation; PEEP = positive end-expiratory pressure; Pplat = plateau pressure. * Days receiving NIV or NHF before intubation. † Days on IMV before enrollment in the study. ‡ ARF days were defined as days from the onset of respiratory failure with any form of ventilatory support until enrollment in the study. § Driving pressure was the difference between the plateau pressure and total PEEP, measured at 6 ml/kg of Vt. || Crs was calculated as Vt divided by the difference between the plateau pressure and total PEEP. ¶ Received at least one session of prone positioning. ** Suspected tension pneumothorax. The worst values for gas exchange and respiratory mechanics are reported in Table 1 (“worst” meaning lowest PaO2 /Fi O2 , highest driving pressure, or lowest respiratory system compliance). Neither complete airway closure nor auto-PEEP was found in any patient. Among the 12 patients, 10 (83%) were poorly recruitable (R/I ratio, 0.21 ± 0.14) on the first day of observation. As shown in Figure 1, patients who did not receive prone positioning had persistent poor recruitability (only 1 out of 17 daily measurements showed high recruitability). In contrast, alternating the body position between supine and prone positioning was associated with increased lung recruitability (13 out of 36 daily measurements showed high recruitability; P = 0.020 by chi-square test between two groups). Prone positioning is indicated as an upside-down triangle in Figure 1. In patients who received prone positioning, PaO2 /Fi O2 went from 120 ± 61 mm Hg at supine to 182 ± 140 mm Hg at prone (P = 0.065 by paired t test). Figure 1. Daily measurements of the recruitment-to-inflation (R/I) ratio for each patient during the observation days. Each patient is indicated by a distinct color. (A) Five patients who did not receive prone positioning. Each triangle denotes a measurement in the supine position. (B) Seven patients who received at least one session of prone positioning. Each upside-down triangle denotes a measurement in the prone position. Notice that each session of prone positioning was maintained for 24 hours. The dashed line represents the cutoff of the R/I ratio for defining lung recruitability (R/I ratio ≥ 0.5 suggests highly recruitable). Discussion This is the first study to describe respiratory mechanics and lung recruitability in a small cohort of mechanically ventilated patients with SARS-CoV-2–associated ARDS. The main findings may be important for clinical management and can be summarized as follows: 1) none of the enrolled patients had complete airway closure or auto-PEEP, 2) driving pressure was high and respiratory system compliance was low, and 3) a majority of the patients were poorly recruitable, with high PEEP, but the recruitability seemed to change when alternating body positions were used. Our findings are not generalizable to all cases of SARS-CoV-2–associated ARDS. First of all, the sample was small (n = 12) and nonrandom. The patients had severe disease and on average had 22 cm H2O of driving pressure despite using 6 ml/kg Vt. Although we were not able to compare the recruitability measured by the R/I ratio with that assessed by another technique (e.g., computed tomography), the low R/I ratio at Day 1 seemed consistent with the clinical impression of the clinicians. Of note, these patients had received various durations of noninvasive and invasive mechanical ventilation, and it would have been ideal to obtain these measurements as soon as the patients were intubated. The surprising finding that alternating body position is followed by increased lung recruitability is interesting but needs to be confirmed. The improvement in oxygenation with prone positioning was not statistically significant but seemed to be clinically relevant. Three patients received both prone positioning and extracorporeal membrane oxygenation, which may also affect lung recruitability (7). During our clinical practice, PEEP was set at the clinicians’ own discretion. However, once the R/I ratio was determined, 5–10 cm H2O of PEEP was usually used if the patient was poorly recruitable. In highly recruitable patients, a higher PEEP was used as long as the plateau pressure was tolerable. In conclusion, our data show that lung recruitability can be assessed at the bedside even in a very constrained environment and was low in our patients with COVID-19–induced ARDS. Alternating body positioning improved recruitability. Our findings do not imply that all patients with SARS-CoV-2–associated ARDS are poorly recruitable, and both the severity and management of these patients can differ remarkably among regions. Instead, we think these findings might prompt clinicians to assess respiratory mechanics and lung recruitability in this population.
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                Author and article information

                Journal
                Am J Respir Crit Care Med
                Am. J. Respir. Crit. Care Med
                ajrccm
                American Journal of Respiratory and Critical Care Medicine
                American Thoracic Society
                1073-449X
                1535-4970
                15 August 2020
                15 August 2020
                15 August 2020
                15 August 2020
                : 202
                : 4
                : 604-606
                Affiliations
                [ 1 ]Johns Hopkins University School of Medicine

                Baltimore, Maryland
                Author notes
                [*]

                These authors contributed equally to this work.

                [ ]Corresponding author (e-mail: mdamarl1@ 123456jhmi.edu ).
                Author information
                http://orcid.org/0000-0002-5091-1975
                Article
                202004-1331LE
                10.1164/rccm.202004-1331LE
                7427393
                32551807
                e4b00530-7f78-41bb-9f9f-cacab9aeaccd
                Copyright © 2020 by the American Thoracic Society

                This article is open access and distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives License 4.0 ( http://creativecommons.org/licenses/by-nc-nd/4.0/). For commercial usage and reprints, please contact Diane Gern ( dgern@ 123456thoracic.org ).

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