By Jane Guttendorf, DNP, CRNP, ACNP-BC, CCRN
Assistant Professor, Acute & Tertiary Care, University of Pittsburgh, School of Nursing
An early trial of prone positioning in patients with acute respiratory distress syndrome (ARDS) demonstrated improved oxygenation but no mortality benefit.1 Then in 2013, Guérin et al documented improved outcomes with proning in patients with severe ARDS (PROSEVA trial).2 This trial randomized 466 subjects early after initiation of mechanical ventilation to either a prone or supine group. Patients in the study group were proned for at least 16 hours daily for a mean duration of 4 ± 4 days. Mortality at day 28 was significantly lower in the prone vs. supine group (16% vs. 33%, respectively, P < 0.001).2 Early proning of patients with severe ARDS has become standard of care, and following the protocol of the PROSEVA trial, long periods of proning are instituted (16 or more hours per day for multiple consecutive days). Initiation of early nutritional support, even during prone positioning, is important because early institution of enteral nutrition (EN) is associated with reduced mortality, shorter hospital length of stay, and lower rates of infection.3,4
The 2016 guidelines for nutritional therapy in critically ill patients published by the Society of Critical Care Medicine and the Association of Parenteral and Enteral Nutrition include:
• assessing patients on admission to the intensive care unit (ICU) for nutrition risk;
• calculating both energy and protein requirements to determine goals of nutrition therapy;
• initiating EN within 24-48 hours of the onset of critical illness and admission to the ICU, with an aim to increase to goal rates over the first week of ICU stay;
• reducing the risk of aspiration or improving tolerance to gastric feeding (by the use of prokinetic agents, continuous infusion, chlorhexidine mouthwash, elevating the head of bed, and diverting level of feeding in the gastrointestinal tract);
• implementing enteral feeding protocols;
• avoiding the use of gastric residual volumes as part of routine care to monitor ICU patients on EN; and
• starting parenteral nutrition early when EN is not feasible or sufficient in high-risk or poorly nourished patients.5
Nutritional therapy for proned patients should follow the same guidelines and recommendations, although there is heightened concern for nasogastric (NG) tube displacement during proning, increased abdominal pressure, which may promote regurgitation and vomiting, and impaired gastric emptying due to the increased use of sedative medications in these patients, many of whom are receiving neuromuscular blockade (NMB) as part of their management of severe ARDS.
Enteral Nutrition in Proned Patients Prior to COVID-19
An early study of critically ill patients to determine tolerance of EN, as measured by gastric residual volumes (GRV), used a crossover design where patients were evaluated for six hours in the prone position, then six hours in the supine position (or vice versa).6 There was no significant difference in mean GRV after three hours of feeding in both supine and prone positions (59.5 mL vs. 59.7 mL), or after six hours (median GRV 95 mL, range 10 mL to 340 mL vs. median GRV, 110 mL; range, 0 mL to 325 mL). The authors concluded that enteral feeding could be continued for patients in the prone position.6
In contrast, Reignier et al found that EN was poorly tolerated in critically ill mechanically ventilated patients.7 Proned patients (n = 34) had the head of the bed slightly elevated and were turned every six hours; when supine, they were in a semi-recumbent position. The supine group (n = 37) remained in a semi-recumbent position. All patients received EN via NG tube for 18 hours per day. Prone position patients had significantly greater GRV and experienced more vomiting episodes. EN was stopped in 82% of prone patients and 49% of supine patients (P < 0.01).7
A follow-up study by Reignier et al showed improved tolerance of EN in proned patients using a different protocolized approach.8 This before-after study used a similar protocol to that described earlier as the “before” phase (control group, n = 34). EN was given for 18 hours/day; if patients were on insulin therapy, it was given continuously. EN was started at 30 mL/hour and increased by 30 mL/hour each subsequent day until day 5. For the intervention phase (n = 38), a standardized ICU protocol for early EN had been instituted and included head of bed elevation to 25 degrees while in the prone position and continuous delivery of EN over 24 hours per day starting at 25 mL/hour and increasing by 25 mL/hour every six hours to a target of 85 mL/hour. Additionally, all proned patients received erythromycin 250 mg intravenous (IV) every six hours as a prokinetic agent, beginning with the first turn to prone position. Patients in the intervention group had greater median volumes of EN for each of five study days. There were no significant differences in GRV and vomiting between groups, with intolerance to EN occurring in 71% of control patients and 63% of intervention patients.8
A single-center study in Madrid enrolled 34 patients over three years to evaluate the feasibility and efficacy of EN in patients receiving mechanical ventilation and prone positioning.9 EN was administered via NG tube, delivered continuously, and titrated up according to protocol over four days to achieve the goal of 25 kcal/kg/day. No prokinetic agents were used routinely. The prone session was planned to last 48 hours using reverse Trendelenburg position. Mean days of EN were 24.7 ± 12.3. Mean days with EN while supine (21.1 days) were significantly higher than while proned (3.7 days, P < 0.01), although there were no significant differences in nutrient delivery, GRV, vomiting, or regurgitation between supine and prone days.9
More recently, Savio et al reported on the feasibility and effectiveness of EN in 47 ARDS patients with prone positioning.10 While supine, the head of the bed was elevated to 30 degrees; while prone, a 15-degree reverse Trendelenburg position was used. All patients had EN delivered via NG or orogastric (OG) tube, continuously, with GRV measurement every six hours. Prokinetics were not used routinely but could be prescribed if needed. The EN rate was adjusted according to GRV. For GRV 250 mL to 300 mL, 250 mL was returned, then EN rate adjusted down. If GRV was > 300 mL, EN was held for one hour and resumed at a reduced rate, and a prokinetic agent was recommended. The average duration of proning was 46.8 hours. There were no significant differences in calories received during proning and supination; however, patients received a higher percentage of prescribed protein in supine as compared to prone position (P = 0.02). Feeding was interrupted 12.3% of prone hours vs. 24.1% of supine hours (P = 0.344). There were no differences in intolerance (vomiting or diarrhea) between groups. The mean GRV was 5.3 mL during prone hours vs. 15.1 mL during supine hours (P = 0.03), although neither was considered a clinically significant volume. EN while prone was feasible and well-tolerated, and the nutritional delivery of calories and protein was comparable to that in the supine position.10
A recent systematic review on this topic included three studies reviewed here and two others: one enrolled 25 adults with ARDS, and the other enrolled 35 preterm infants.6,7,9,11 The primary outcome evaluated was GRV. There were mixed results with regard to GRVs and vomiting, with no evidence of increased risk of pneumonia or death.11 Another systematic review concluded that there was no difference in clinically significant outcomes, but EN delivered by continuous infusion appeared to be better tolerated.12
One study suggests a dose-response for early EN in patients with high nutritional risk (mNUTRIC score) and moderate to severe ARDS requiring prolonged prone positioning.13 The duration of proning was 48 hours. EN was provided as continuous infusion via NG tube beginning on day 1 of ICU admission. Target energy was 20 kcal/kg/day to 25 kcal/kg/day, and target protein intake was 1.2 gm/kg/day. Energy achievement rate (EAR) was measured daily for seven days beginning at the start of prone positioning (in an earlier trial, an EAR > 65% was found to be a good prognostic factor). Seventy-nine patients were included, 38 died, and 41 survived. EAR during the first week of ICU admission was significantly different between survival and nonsurvival groups (P = 0.004). Additionally, in the survival group, EAR significantly increased during the post-prone positioning phase (days 4-7), whereas only a minimal increase in EAR was noted in the nonsurvival group (median EAR 77.9% vs. 51.1%, respectively, P = 0.025). By multivariate analysis, EAR was a strong predictor for ICU mortality (hazard ratio [HR], 0.19; 95% confidence interval [CI], 0.07-0.56). The authors recommended that early EN and increasing EAR > 65% may benefit ARDS patients at high nutritional risk who require prolonged prone positioning.13
Enteral Nutrition in Proned Patients with COVID-19
The overwhelming number of COVID-19 ARDS patients has refocused attention on maintaining low tidal volume ventilation and rescue therapies for severe hypoxemia, including early and prolonged prone positioning, use of neuromuscular blocking agents, and use of heavy sedation. This, in turn, has brought the discussion of EN in proned patients back into sharp focus. Additional considerations in the management of nutrition therapy in COVID-19 patients include the need to limit exposure to patients considered infectious, maintain compliance with Centers for Disease Control and Prevention guidelines for infection control, minimize aerosolizing procedures, conserve personal protective equipment (PPE), and coordinate care among team members.
During the past two years, several studies have been published evaluating EN in COVID-19-related ARDS, specifically examining EN use in the prone position. An international one-day point-prevalence study evaluated nutrition practices in patients with and without COVID-19 in 135 ICUs. Analysis included 1,229 patients. Patients were divided into COVID-19 (n = 602) and non-COVID-19 (n = 607) groups, and delivery of nutrition was evaluated. A higher proportion of COVID-19 patients received EN compared to non-COVID patients (69% vs. 50%, P < 0.0001); and a higher proportion of mechanically ventilated COVID-19 patients received EN compared to mechanically ventilated non-COVID-19 patients (81.7% vs. 67.3%; P < 0.0001). Compared to non-COVID-19 patients, a higher proportion of COVID-19 patients received energy ≥ 20 kcal/kg/day (55% vs. 45%, P = 0.0007) and protein ≥ 1.2 gm/kg/day (45% vs. 35%, P = 0.0011).14
Two single-center retrospective studies evaluated nutrition in COVID-19 patients.15,16 In the study by Alencar et al, prone positioned patients (n = 54) received lower energy, protein, and total calories using EN compared with supine positioned patients (n = 58). While proned, patients were in 15-degree reverse Trendelenburg, prokinetic agents were used, and patients had enteral diet breaks immediately before and following a proning maneuver. Mortality was 87.5%.15 Miguelez et al reported on 176 COVID-19 patients, predominantly male (73%), over a two-month period. The majority of patients required prone positioning (89%).16 Patients received predominantly parenteral nutrition or a combination of parenteral and enteral nutrition. At days 4 and 7, 10% and 17% of patients, respectively, received exclusively EN, compared to 82% of patients at day 4 and 80% of patients at day 7 on parenteral nutrition only. ICU mortality was 36.4%.16
Several groups have published nutrition therapy guidelines for critically ill patients with COVID-19, mostly based on extrapolation of data from the management of other ARDS patients and general nutrition therapy guidelines for critically ill patients. Martindale et al recommend strategies to reduce exposure and spread of disease by providing clustered care and use of personal protective equipment.17 EN should be initiated early using a standard isosmolar polymeric formula, starting at trophic doses and advancing as tolerated. They noted that intragastric EN can be provided safely even during prone positioning.17 Similarly, Chapple et al provided guidelines for nutrition management of critically and acutely ill patients with COVID-19 in Australia and New Zealand.18 These were developed using primarily expert consensus. They recommended nutrition care should be tailored to pandemic capacity. In addition, they recommended early gastric feeding in low-nutritional-risk patients, measuring GRV every eight hours, turning feeds off and aspirating the tube prior to each proning maneuver, and advancing to goal energy by day 5 of ICU admission. For high-nutritional-risk patients, they recommended early consultation with a dietitian prior to beginning EN and earlier advancement of feeds to goal (by day 3). Prokinetics could be used for intolerance or high GRV.18
Overall, the guidelines for providing nutrition therapy to prone positioned patients does not differ from the standard of care for supine patients. In comparison to the very early reports of EN in proned patients, it seems useful to use reverse Trendelenburg position while prone, to initiate EN early (within 24-48 hours of ICU admission once the patient is hemodynamically stable and lactate is improving), to deliver EN continuously over 24 hours via NG or OG tube, to target energy goals of 25 kcal/kg/day to 30 kcal/kg/day and protein goals of 1.2 gm/kg/day to 2 gm/kg/day (see guidelines for energy and protein targets for obese patients).
It is important to emphasize that while GRV was used as a measure of tolerance of enteral feedings in the early studies of prone patients, current guidelines recommend against routine use of GRV to assess tolerance of EN because GRV does not correlate with incidence of pneumonia, regurgitation, or aspiration.5 Alternate strategies that may be useful in critically ill patients for assessing tolerance of EN include physical examination, review of abdominal radiologic films to evaluate tube position and for evidence of ileus, and evaluation of clinical risk factors for aspiration.5 Consider the addition of prokinetic agents when necessary for patients not tolerating gastric feeding.
REFERENCES
- Gattinoni L, Tognoni G, Pesenti A, et al. Effect of prone positioning on the survival of patients with acute respiratory failure. N Engl J Med 2001;345:568-573.
- Guérin C, Reignier C, Richard J-C, et al. Prone positioning in severe acute respiratory distress syndrome. N Engl J Med 2013;368:2159-2168.
- Artinian V, Krayem H, DiGiovine B. Effects of early enteral feeding on the outcome of critically ill mechanically ventilated medical patients. Chest 2006;129:960-967.
- Marik PE, Zaloga GP. Early enteral nutrition in acutely ill patients: A systematic review. Crit Care Med 2001;29:2264-2270.
- Taylor BE, McClave SA, Martindale RG, et al. Guidelines for the provision and assessment of nutrition support therapy in the adult critically ill patient: Society of Critical Care Medicine (SCCM) and American Society for Parenteral and Enteral Nutrition (A.S.P.E.N.). Crit Care Med 2016;44:390-438.
- van der Voort PH, Zandstra DF. Enteral feeding in the critically ill: Comparison between the supine and prone positions: A prospective crossover study in mechanically ventilated patients. Crit Care 2001;5:216-220.
- Reignier J, Thenoz-Jost N, Fiancette M, et al. Early enteral nutrition in mechanically ventilated patients in the prone position. Crit Care Med 2004;32:94-99.
- Reignier J, Dimet J, Martin-Lefevre L, et al. Before-after study of a standardized ICU protocol for early enteral feeding in patients turned in the prone position. Clin Nutr 2010;29:210-216.
- Saez de la Fuente I, Saez de la Fuente J, Quintana Estelles MD, et al. Enteral nutrition in patients receiving mechanical ventilation in a prone position. JPEN J Parenter Enteral Nutr 2016;40:250-255.
- Savio RD, Parasuraman R, Lovesly D, et al. Feasibility, tolerance and effectiveness of enteral feeding in critically ill patients in prone position. J Intensive Care Soc 2021;22:41-46.
- de Souza Machado L, Rizzi P, Silva FM. Administration of enteral nutrition in the prone position, gastric residual volume and other clinical outcomes in critically ill patients: A systematic review. Rev Bras Ter Intensiva 2020;32:133-142.
- Bruni A, Garofalo E, Grande L, et al. 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.
- Fu PK, Wang CY, Wang WN, et al. Energy achievement rate is an independent factor associated with intensive care unit mortality in high-nutritional-risk patients with acute respiratory distress syndrome requiring prolonged prone positioning therapy. Nutrients 2021;13:3176.
- Nakamura K, Liu K, Katsukawa H, et al. Nutrition therapy in the intensive care unit during the COVID-19 pandemic: Findings from the ISIIC point prevalence study. Clin Nutr 2021;Sep 27:S0261-5614(21)00450-7.
- Alencar ES, Muniz LSDS, Holanda JLG, et al. Enteral nutritional support for patients hospitalized with COVID-19: Results from the first wave in a public hospital. Nutrition 2021:11;94:111512.
- Miguélez M, Velasco C, Camblor M, et al. Nutritional management and clinical outcome of critically ill patients with
COVID-19: A retrospective study in a tertiary hospital. Clin Nutr 2021; Nov 1:S0261-5614(21)00499-4. - Martindale R, Patel JJ, Taylor B, et al. Nutrition therapy in critically ill patients with coronavirus disease 2019. J Parenter Enteral Nutr 2020;44:1174-1184.
- Chapple LS, Fetterplace K, Asrani V, et al. Nutrition management for critically and acutely unwell hospitalised patients with coronavirus disease 2019 (COVID-19) in Australia and New Zealand. Aust Crit Care 2020;33:399-406.
The author reviews the use of enteral nutrition in critically ill patients during prone positioning.
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