A guide to enteral nutrition in intensive care units: 10 expert tips for the daily practice

The preferential use of the oral/enteral route in critically ill patients over gut rest is uniformly recommended and applied. This article provides practical guidance on enteral nutrition in compliance with recent American and European guidelines. Low-dose enteral nutrition can be safely started within 48 h after admission, even during treatment with small or moderate doses of vasopressor agents. A percutaneous access should be used when enteral nutrition is anticipated for ≥ 4 weeks. Energy delivery should not be calculated to match energy expenditure before day 4–7, and the use of energy-dense formulas can be restricted to cases of inability to tolerate full-volume isocaloric enteral nutrition or to patients who require fluid restriction. Low-dose protein (max 0.8 g/kg/day) can be provided during the early phase of critical illness, while a protein target of > 1.2 g/kg/day could be considered during the rehabilitation phase. The occurrence of refeeding syndrome should be assessed by daily measurement of plasma phosphate, and a phosphate drop of 30% should be managed by reduction of enteral feeding rate and high-dose thiamine. Vomiting and increased gastric residual volume may indicate gastric intolerance, while sudden abdominal pain, distension, gastrointestinal paralysis, or rising abdominal pressure may indicate lower gastrointestinal intolerance.

Introduction

The importance of nutrition in the critically ill is increasingly acknowledged, especially in patients with long stay in the intensive care unit (ICU), who often require prolonged life-sustaining support and go through a state of severe catabolism [1, 2]. Some aspects of the nutrition practice such as the preferential use of the early oral/enteral nutrition (EN) over «gut rest» and the acceptance of delaying provision of amounts of nutrients calculated to match the losses and expenditure, while other aspects can raise controversial views [3,4,5].

International guidelines have been recently updated by the American Society of Parenteral and Enteral Nutrition/Society of Critical Care Medicine [6] and the European Society of Clinical Nutrition and Metabolism (ESPEN) [2, 7], with various levels of supporting evidence (Table 1). A group of experts in critical care nutrition from different regions of the world was commissioned to discuss some of the practicalities of early EN, listed in Table 1 and supported in the corresponding sections, to use and to complement the guidelines [6, 7] by providing tips inspired by the current knowledge and clinical experience of the experts. Importantly, nutritional requirements will vary according to the phase of critical illness, our tips are general in nature, and an individualized approach should always be used.

figure 1

Current data consistently demonstrate that ICU patients receive low amounts of protein (average of 0.6 g/kg/day for the first two weeks) [24, 60,61,62,63,64,65,66,67]. Higher protein provision is associated with reduced mortality in adults in observational trials [61, 68,69,70,71,72,73,74], biochemical outcome parameters and morphometric outcomes in skeletal muscle [75,76,77,78,79], improved quality of life at 3-month post-ICU [69] or handgrip strength at hospital day 7 and muscle mass [73]. However, prospective studies show limited effects on clinical, patient-centered and functional outcomes or yield negative results [45, 67, 74,75,76,77,78,79,80,81]. Admittedly, a limited number of large RCTs examined clinical outcomes of specifically increasing protein administration.

Hence, there is no evidence for a higher protein intake in critically ill patients in terms of clinically relevant outcomes in prospective randomized trials [82, 83]. Moreover, some harm can be related to excessive amounts of proteins in a post hoc analysis of prospective trials performed in adults [45, 84, 85] or in children [86] and in a retrospective study [87]. Hence, it may be prudent to start protein delivery at a lower dose (~ 0.8 g/kg) and ramp up protein dose to the targeted protein goal (> 1.2–1.3 g/kg/day [6, 7] (Fig. 2). However, this strategy was not previously evaluated in prospective studies.

figure 2

The role of high-protein intakes that stress the need for focused larger clinical trial evidence examining the effect of specifically increasing protein delivery [4, 67, 84], combined with active mobilization to optimize physical therapy and functional outcomes in long-stayers, requires further study. Importantly, muscle volume and strength are not necessarily related. Preliminary data suggest that the combination of neuromuscular electrical stimulation and high-protein supplementation (1.8 g/kg/day) significantly improved short physical performance [88]. The role of high-dose protein delivery and in-bed ergometry (cycling) is being meaningfully studied [89] (NCT03021902).

Question 7: When should hyperprotein formulas be used?

There now exist a range of available high protein-to-energy ratio products intended to meet protein targets and non-protein calorie goals with a limited risk of overfeeding of non-protein calories. The use of enteral protein supplements or supplemental amino acid solutions (such as clear liquid whey protein formulas) is proposed for this purpose [90]. However, it is important to keep the amino acid composition well balanced. Nutrition regimens that are grossly unbalanced inflict a metabolic strain on the patient [91]. A high-protein product may be used in the later stable phase of critical illness [85]. However, there are no data from prospective randomized controlled studies with clinically relevant outcomes to support this recommendation.

Some potential alternatives include the addition of the leucine metabolite HMB (hydroxy methyl butyrate) to improve amino acid metabolism and reduce net protein breakdown [92].

A high-nitrogen intake should always be accompanied by daily monitoring of plasma concentration of urea and creatinine together with base excess. If plasma urea concentration is increasing, urea excretion in urine should be identified and followed by a decrease of protein intake and eventually renal replacement therapy. If base excess increases, always consider reducing protein intake. Acidosis may come in critically ill patients for several reasons, but when the renal compensatory mechanisms are overridden will the ability to eliminate a surplus of nitrogen be impaired.

Question 8: When and how to start micronutrients?

Ingestion of micronutrients (MN), i.e., trace elements and vitamins, is essential for normal metabolism [93], immunity [94], and antioxidant defense. They work as a web, and 24 of them are "essential," meaning that nutrition is the only source. The body stores of MNs are variable but generally insufficient to ensure normal metabolism beyond one week. The MNs needs will depend on the presence of prior deficiency, food intake before admission, particular body fluid losses, disease, and feeding rate. The available feeding products are meant to cover the needs of healthy people (dietary reference intakes) provided about 1500 kcal/day is delivered to the patients [95]. However, these amounts are not integrating the specific requirements of critically ill patients. Intestinal function and absorption are often absent or depressed during the first days, and antioxidant stress is maximal [96].

Further, most recent guidelines [7] recommend that EN is started within 48 h of admission after stabilization [5] and progressed to target over 3–4 days (Fig. 2). Consequently, MN delivery starts at close to zero and remains below DRI for nearly a week, or "forever" in patients receiving less than 1500 kcal. It has been proposed to measure blood concentrations of some MN at risk [15]. The results of analysis are often not timely available and may be costly. As most patients stay briefly (< 5 days), there is no time to adapt to a delayed abnormal result. Nevertheless, blood values determination is rational for selected MNs depending on pathology and treatment when the patients stay more than a week, especially when renal replacement therapy is required [97,98,99,100,101].

Critically ill patients are often admitted with a nutritional deficit developed in the days preceding ICU admission, translating into MN deficiencies. The earliest manifestation is refeeding syndrome (RFS), with thiamine being in the first line discussed below [105]. The late complications are less specific, generally unrecognized, and sometimes called an "invisible foe" [110, 102,103,104,105]. Infections and wound healing complications are in the first line as MN are essential for immune defense. Therefore, during the early phase, as EN cannot cover the everyday needs and the higher needs associated with critical illness, early intravenous delivery of doses like those used in PN is rational (1 vial multitrace element and multivitamin + 100–200 mg thiamine) (Fig. 2). A few trials have shown that the strategy to deliver MNs intravenously at doses 4–5 times higher than for PN until EN can cover the needs is associated with better global outcomes [106, 107].

Question 9: How to screen and manage patients for refeeding syndrome?

Refeeding syndrome (RFS) is a potentially fatal acute metabolic response following the reintroduction of nutrients after a variable length of starvation that may lead to morbidity and increased mortality [108].

Refeeding syndrome is characterized by electrolyte shifts that arise from a switch from a catabolic state using fat and protein as energy sources back to carbohydrate metabolism. Glucose substrate utilization leads to increased insulin levels, resulting in thiamine depletion and low plasma levels of phosphate, magnesium and potassium due to the intracellular shift of electrolytes [109,110,111]. The complications of RFS are so severe that the liberal administration of intravenous thiamine 100–200 mg/day for the first 3 days should be part of routine (Fig. 2). In the absence of appropriate management, many clinical potentially life-threatening consequences may develop [108].

Recent studies have demonstrated that high-energy intake during RFS is associated with increased mortality, and caloric restriction confers improved outcomes [114, 115]. The difference in mortality occurred much later during patients’ ICU stay after correction of electrolyte imbalance, suggesting a complex pathophysiology [41, 114]. Thiamine administration and caloric restriction of 500 kcal/day or 25% of the estimated target inspired from NICE guidance [116] is a frequent practice for ICU patients with hypoP/RFS for at least 48 h.

Practical protocols are available on-line (e.g., [117]) to guide progressing energy to target in the early phase of ICU stay is provided. Energy target on admission is based on predictive equations. In 4 steps of 25%, feeds are advanced to the estimated target to prevent overfeeding, including non-nutritional energy from propofol and citrate. Indirect calorimetry is performed to adjust to the actual energy expenditure and set as a new target. When refeeding hypoP within 72 h after the start of EN is encountered, caloric restriction is warranted. After 48 h subsequently, the following steps (25%) are set.

Question 10: How to assess gastrointestinal intolerance?

Gastrointestinal (in)tolerance is often defined with certain symptoms/signs, with ‘tolerance’ meaning the absence of these symptoms and signs [118,119,120]. ‘Enteral feeding intolerance’ (EFI) is commonly defined as a certain amount of gastric residual volumes (GRV) [119,120,121], capturing only upper gastrointestinal (GI) problems after initiation of enteral tube feeding, while both upper and lower parts of the GI tract can be involved (Fig. 3). In most of available studies, patients with EFI were more severely ill compared to patients tolerating EN, suggesting that EFI could be an epiphenomenon or a marker of disease severity [118]. In several studies, the occurrence of EFI as a feature of GI dysfunction was shown to independently associate with adverse outcome, as an additional organ dysfunction [119, 121,122,123,124].

figure 3

Gastric intolerance assessed by the GRV measurement is the prevalent gastrointestinal symptom in ICU patients treated with EN [118, 125, 126]. Measurements of GRV have been omitted in many sites since a study showed no benefit of GRV-guided EN in patients with already established EN despite vomiting occurred more often in patients without than with GRV measurements [127]. However, the relation of GRV with the tracheal aspiration of gastric contents and pneumonia development is not clear [128, 129] and GRV measurement is a time-consuming practice and is associated with infectious risk (COVID-19) and variability in practices [121, 122]. Due to these factors and uncertainties, recent guidelines either do not recommend routine measurement of GRV [6], or suggest restricting GRV measurements to the initiation and progression of EN only [5, 7]. The latter is important, as evidence from RCTs is available only for medical patients having full EN already established at study inclusion [126]. Moreover, there is no good substitute for GRV, which could be considered as a surrogate marker of gastric emptying at bedside [128]. Therefore, depending on local constraints, GRV can still be included in assessment of EFI and a GRV over 500 ml/6 h is considered as an indication for intervention (delay or interruption of EN or application of prokinetics) [129]. [5, 7, 130,131,132,133], even though prokinetics has not been proven to improve patient-relevant outcomes [134].

Lower parts of GI tract are often involved, even in the absence of upper GI intolerance. Lower GI intolerance requires different management. Bowel paralysis leading to bowel distension in patient receiving EN may be associated with adverse outcomes. Patients in shock receiving early full EN compared to PN more often developed Ogilvie’s syndrome and bowel ischemia [22]. Monitoring and management of EFI and GI dysfunction is complicated due to the lack of robust and reproducible markers and multifaceted clinical presentation [49]. As no single straightforward marker reliably detects GI dysfunction, using composite scores combining several symptoms and signs could be helpful and should be considered [131]. EFI at the bedside is defined as features of GI dysfunction appearing during EN and consequently leading to reduction or discontinuation of EN. [123, 124, 135] Evidence on management options, unanswered issues and proposals for future research on GI dysfunction have been recently summarized [136]. In brief, patients should be carefully assessed for high gastric residual volume (optional—threshold 500 ml/6 h), vomiting, pain, distension, elevated/increasing intra-abdominal pressure, GI paralysis.

Conclusions

The importance of medical nutrition in the care of the critically ill cannot be overstated. Overall, the management of EN requires a systematic and updated approach involving all ICU professionals, including practical approaches proposed in this document and regular updates. Auditing changes in practice are needed locally from the entire community of ICU professionals to increase the safety and efficiency of the delivery of EN.

Availability of data materials

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Authors and Affiliations

  1. Erasme University Hospital, Université Libre de Bruxelles, 808 Route de Lennik, 1070, Brussels, Belgium Jean-Charles Preiser
  2. Intensive Care Department, College of Medicine, King Saud Bin Abdulaziz University for Health Sciences and King Abdullah International Medical Research Center, Ministry of National Guard Health Affairs, Riyadh, Saudi Arabia Yaseen M. Arabi
  3. Adult Intensive Care, Lausanne University Hospital, CHUV, 1011, Lausanne, Switzerland Mette M. Berger
  4. Clinical Department and Laboratory of Intensive Care Medicine, Department of Cellular and Molecular Medicine, Katholieke Universiteit Leuven, Leuven, Belgium Michael Casaer & Greet Van den Berghe
  5. Department of Medicine, University of Louisville School of Medicine, Louisville, KY, USA Stephen McClave
  6. Intensive Care Medicine, Hospital Universitario, 12 de Octubre, Instituto de Investigación imas12, Madrid, Spain Juan C. Montejo-González
  7. Department of Intensive Care Medicine, The Queen Elizabeth Hospital, Woodville, SA, Australia Sandra Peake
  8. Department of Critical Care Research, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, Australia Sandra Peake
  9. Department of Intensive Care Medicine, Lucerne Cantonal Hospital, Lucerne, Switzerland Annika Reintam Blaser
  10. Department of Anaesthesiology and Intensive Care, University of Tartu, Tartu, Estonia Annika Reintam Blaser
  11. Ede and Division of Human Nutrition and Health, Gelderse Vallei Hospital, Wageningen University and Research, Wageningen, The Netherlands Arthur van Zanten
  12. Division of Anaesthesiology and Intensive Care Medicine, Department of Clinical Science, Intervention and Technology, Karolinska Institutet, Stockholm, Sweden Jan Wernerman
  13. Department of Anesthesiology and Surgery, Duke University School of Medicine, Durham, NC, USA Paul Wischmeyer
  1. Jean-Charles Preiser
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Contributions

JCP drafted the conception and design of this article, YMA drafted Sects. 1 and 2, SMC drafted Sect. 3, MC and GVdB drafted Sect. 4, SP drafted Sect. 5, PW and JW drafted Sects. 6 and 7, MB and AvZ drafted Sects. 8 and 9, and ARB and JCM drafted Sect. 10. All authors critically revised the manuscript and brought significant contributions to all sections. All authors read and approved the final manuscript.

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Competing interests

Jean-Charles Preiser: speaker’s and consultant’s fee form Baxter, DIM-3, Fresenius, Nestlé HealthScience, Nutricia/Danone, VIPUN. Yaseen M. Arabi: Principal investigator on an investigator-initiated RCT for protein intake in critically ill patients (NCT04475666). Mette M. Berger: speaker fees from Abbott, Baxter, BBraun, DSM, Fresenius Kabi, Nestlé HealthScience, Nutricia/Danone. Michael Casaer: supported by the Research Foundation—Flanders, Belgium (Fundamental Clinical Research fellowship 1700111N;) and a KULeuven C2 Research Project Grant (C24/17/070) and received a speaker fee from Fresenius (°2020) and a consultant fee from Baxter (°2021). Stephen McClave,: none declared. Juan Carlos Montejo: speaker’ and consultant’s fees and research grants from Abbott, Baxter, Fresenius-Kabi, GE Healthcare, Nestlé HealthScience. Sandra Peake: none declared. Annika Reintam Blaser received speaker or consultancy fees from Fresenius Kabi, Nestlé and VIPUN Medical. University of Tartu received a study grant from Fresenius Kabi. ARB is one of the authors of ESICM guidelines on early enteral nutrition; ESPEN guidelines on clinical nutrition in the intensive care nutrition and BMJ rapid recommendations on the prophylaxis of gastrointestinal bleeding in critically ill. Greet Van den Berghe: funded by the Methusalem program of the Flemish Government (METH/08/07 which has been renewed as METH/14/06 via KU Leuven); the European Research Council (ERC) Advanced Grants (AdvG-2012-321670 from the Ideas Program of the EU FP7 and AdvG-2017-785809 from the Horizon 2020 Program of the EU) Greet Van den Berghe has no conflict of interest regarding this publication. Arthur van Zanten: speaker’ and consultant’s fees and research grants from Abbott, AOP Pharma, BBraun, Cardinal Health, Baxter, DIM-3, Fresenius-Kabi, GE Healthcare, Mermaid, Lyric, Nestlé HealthScience, Nutricia/Danone, Rousselot. Jan Wernerman: speaker’s fees from GE Healthcare, Nestlé and Nutricia Danone, no conflict of intrest regarding this publication. Paul Wischmeyer: Dr. Wischmeyer reports receiving investigator-initiated grant funding related to this work from National Institutes of Health, Canadian Institutes of Health Research, Abbott, Baxter, and Fresenius. Dr. Wischmeyer has served as a consultant to Abbott, Fresenius, Baxter, Takeda, Gravitas, and Nutricia. Dr. Wischmeyer has received unrestricted gift donation for nutrition research from Musclesound and DSM. Dr. Wischmeyer has received honoraria or travel expenses for CME lectures on improving nutrition care from Abbott, Baxter, Danone-Nutricia and Nestle.

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Preiser, JC., Arabi, Y.M., Berger, M.M. et al. A guide to enteral nutrition in intensive care units: 10 expert tips for the daily practice. Crit Care 25, 424 (2021). https://doi.org/10.1186/s13054-021-03847-4

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