Intensive & Critical Care Nursing xxx (xxxx) xxx

Contents lists available at ScienceDirect

Intensive & Critical Care Nursing

journal homepage: www.elsevier.com/iccn

Review Article

Nursing issues in enteral nutrition during prone position in critically ill

patients: A systematic review of the literature
Andrea Bruni a,1, Eugenio Garofalo a,1, Laura Grande b, Gaetano Auletta c, Davide Cubello a, Manfredi Greco d,
Nicola Lombardo e, Pietro Garieri f, Anna Papaleo g, Patrizia Doldo h, Rocco Spagnuolo i, Federico Longhini a,⇑
a
Anesthesia and Intensive Care, Department of Medical and Surgical Sciences, ‘‘Magna Graecia” University, Catanzaro, Italy
b
Surgery Unit, ‘‘Santa Rita” Clinic, Vercelli, Italy
c
School of Nursing, Department of Translational Medicine, Eastern Piedmont University, Novara, Italy
d
Plastic Surgery Unit, Department of Clinical and Experimental Medicine, ‘‘Magna Graecia” University, Catanzaro, Italy
e
Department of Medical and Surgical Sciences, ‘‘Magna Graecia” University, Catanzaro, Italy
f
Department of Biomedical Sciences for Health, University of Milan, Italy
g
Department of Anaesthesia and Intensive Care, IRCCS Ca’ Granda Maggiore Hospital, Milan, Italy
h
School of Nursing, Department of Clinical and Experimental Medicine, ‘‘Magna Graecia” University, Catanzaro, Italy
i
Department of Clinical and Experimental Medicine, ‘‘Magna Graecia” University, Catanzaro, Italy

a r t i c l e i n f o a b s t r a c t

Article history: Background: Early enteral nutrition (EN) and prone position may both improve the outcome of patients
Received 18 February 2020 affected by moderate to severe Acute Respiratory Distress Syndrome. Recent guidelines suggest to
Revised 2 May 2020 administer early EN also during prone position. However, EN intolerance, such as high residual gastric
Accepted 1 June 2020
volumes, regurgitation or vomiting, may occur during pronation.
Available online xxxx
Aim: This systematic review aims to assess the occurrence of high residual gastric volume, regurgitation or
vomiting episodes, that can be encountered in patients receiving EN during prone position.
Keywords:
Methods: We have conducted a systematic review. We queried three scientific databases (MEDLINE,
Enteral nutrition
Nurse
EMBASE and CINAHL) from inception until November 19, 2019 without language restrictions, using key-
Prone position words and related MeSH terms. All relevant articles enrolling adult patients receiving invasive mechanical
Regurgitation ventilation and evaluating the use of early EN during prone position were included.
Residual gastric volume Results: From 111 records obtained, we included six studies. All studies but one reported no differences
Vomiting with respect to gastric residual volumes between supine and prone positions. A 24-hours EN administration
protocol seems to be better, as compared to an 18-hours feeding protocol. The need to stop EN and vomiting
episodes were higher during prone position, although the rate of high gastric volume was similar between
supine and prone positions. Ventilator associated pneumonia, lengths of stay and mortalities were similar
between supine and prone positions. Only one study reported lower mortality in patients receiving EN
throughout the entire day, as compared to an 18-hours administration protocol.
Conclusion: Protocols should be followed by healthcare providers in order to increase the enteral feeding
volume, while avoiding EN intolerance (such as EN stops, high residual volume, regurgitation and vomiting).
Ó 2020 Elsevier Ltd. All rights reserved.

Implications for clinical practice

 Early enteral nutrition during prone positioning is suggested by the current clinical guidelines; however, it may be affected by some
issues of nursing relevance.
 Nurses should recognise and manage complications and issues related to enteral nutrition during prone positioning, together with
the physicians.
 Defined protocols for enteral feeding during prone position seem to be useful in the patient’s management and care.
⇑ Corresponding author at: Department of Medical and Surgical Sciences, ‘‘Magna Graecia” University, Viale Europa 88100, Catanzaro, Italy.
E-mail address: longhini.federico@gmail.com (F. Longhini).
1
AB and EG equally contributed.

https://doi.org/10.1016/j.iccn.2020.102899
0964-3397/Ó 2020 Elsevier Ltd. All rights reserved.

Please cite this article as: A. Bruni, E. Garofalo, L. Grande et al., Nursing issues in enteral nutrition during prone position in critically ill patients: A system-
atic review of the literature, Intensive & Critical Care Nursing, https://doi.org/10.1016/j.iccn.2020.102899
2 A. Bruni et al. / Intensive & Critical Care Nursing xxx (xxxx) xxx
Introduction
Several decades ago, prone positioning was proposed in
patients with hypoxaemic acute respiratory failure to improve
gas exchange (Piehl and Brown, 1976). When applied early and
for prolonged (>16 hours) sessions, prone position reduces the
28-days mortality in patients affected by Acute Respiratory Dis-
tress Syndrome (ARDS) (Guerin et al., 2013). Although a life saving
procedure, prone positioning may be affected by some complica-
tions, such as nasogastric feeding tube, central venous catheters
or orotracheal tube dislodgements or increased risk for pressure
lesions (Lucchini et al., 2018).
According to the recent guidelines released by the European
Society for Clinical Nutrition and Metabolism (ESPEN), enteral
nutrition (EN) should be considered, in the absence of contraindi-
cations, as early as possible (within the first 48 hours from Inten-
sive Care Unit (ICU) admission) in all critically ill patients, even
in those managed in the prone position (Singer et al., 2019). In
addition, also the European Society of Intensive Care Medicine
(ESICM) recommends that early EN should not be delayed solely
because of prone positioning. Furthermore, ESICM guidelines sug-
gest considering the early use of prokinetics, followed by post-
pyloric feeding, in case of persisting gastric retention (Reintam
Blaser et al., 2017). Indeed, early EN reduces the ICU and hospital
mortality (Artinian et al., 2006), length of stay (Marik and Zaloga,
2001) and infectious complications (Marik and Zaloga, 2001).
Deep sedation, septic shock, haemodynamic impairment,
supine positioning without head elevation and elevated intra-
abdominal pressures are common in mechanically ventilated ARDS
patients during prone position; of note, these factors may alter gas-
tric motility and delay emptying, leading to high residual gastric
volume, regurgitation or vomiting episodes (Linn et al., 2015).
Thus, nursing care is fundamental to monitor and recognise EN
intolerance, in order to implement interventions and to improve
enteral feeding. We have therefore designed this systematic review
of the literature to assess issues of interest that nurses could face in
patients receiving early EN during prone positioning.
Materials and methods
We have conducted this systematic review in accordance with
the Preferred Reporting Items for Systematic reviews and Meta-
Analyses (PRISMA) statement (Liberati et al., 2009).
Search strategy, selection criteria and outcome measures
Three scientific databases (MEDLINE, EMBASE and CINAHL)
were searched from inception until November 19, 2019 without
language restrictions, using keywords and related MeSH terms.
The search strategy is detailed in the Electronic Supplemental
Material (ESM). Controlled vocabulary terms, text words and key-
words were variably combined. Blocks of terms per concept were
created.
We included all relevant articles enrolling adult patients receiv-
ing invasive mechanical ventilation and evaluating the use of early
EN during prone position. We excluded papers with one or more of
the following criteria: published in languages other than English,
Italian, French or Spanish; case report or series; review; systematic
reviews or meta-analysis. References of included papers and
review articles were also examined to identify additional studies
missed during the primary search.
We recorded all the following outcomes, considered issues of
potential interest to nurses: residual gastric volumes, EN fed vol-
ume, need to stop the EN, rate of episodes of vomiting or regurgi-
tation, rate of ventilator-associated pneumonia (VAP) or secondary
Please cite this article as: A. Bruni, E. Garofalo, L. Grande et al., Nursing issues in enteral nutrition during prone position in critically ill patients: A system-
atic review of the literature, Intensive & Critical Care Nursing, https://doi.org/10.1016/j.iccn.2020.102899
infections, ICU and hospital length of stay and mortality. For all
measured outcomes, we considered the definition provided in
every single study included in the review.
Data collection and analysis
Two authors (AB and EG) independently screened the
retrieved records for exclusion by title and, then, by abstract,
according to the inclusion/exclusion criteria. Full-texts of possible
relevant articles were assessed for inclusion/exclusion. Data were
independently extracted by two authors (AB and EG), and col-
lected through a dedicated electronic form, specifically designed
for the present review, on Microsoft Excel (Microsoft Corporation,
Redmond, WA, USA). All disagreements were discussed and, if
necessary, resolved by a third author (FL) at every step of the
process.
Statistical analysis
Data were extracted as reported in the original manuscripts.
The methodological quality of included studies was assessed using
Review Manager software (RevMan 5.3; Nordic Cochrane Centre,
Cochrane Collaboration, Copenhagen, Denmark). We evaluated all
studies for randomised sequence generation, allocation conceal-
ment, blinding of participants and personnel, blinding of outcome
assessment, incomplete outcome data, selective outcome report-
ing, and other bias. Randomised and nonrandomised crossover
studies were assessed according to a modified checklist (Ding
et al., 2015).
Descriptive statistics of individual studies used different sta-
tistical indicators for central tendency and variability, such as
means and standard deviations (SD), whereas absolute and rela-
tive frequencies were adopted for qualitative variables. To show
one single indicator for the quantitative variables we collected,
means (SD) or medians and interquartile ranges [IQR] were used,
as appropriate (Messina et al., 2017, Messina et al., 2018). The
scarcity of data published in the literature and low study quality,
prevented the possibility of conducting a pooled data analysis for
outcomes.
Findings
Study selection
The study selection flowchart is reported in Fig. 1. After
launching the search strategy, 111 titles were identified. Fifteen
duplicated records and 89 citations were excluded on the initial
title and abstract screen. After examination of the remaining
seven full text, six studies have been included in the systematic
review (Lucchini et al., 2017, Reignier et al., 2010, Reignier et al.,
2004, Saez de la Fuente et al., 2016, Sams et al., 2012, van der
Voort and Zandstra, 2001). One article was excluded because it
was a narrative review. Risk of bias assessment is depicted in
Fig. 2.
Study and population characteristics
All included studies are single centred (Lucchini et al., 2017,
Reignier et al., 2010, Reignier et al., 2004, Saez dela Fuente et al.,
2016, Sams et al., 2012, van der Voort and Zandstra, 2001). Design
and characteristics of included studies are reported in Table 1.
Overall, the six studies included 241 patients, with a median of
30 [21–62] patients per study. The median age was 55 [50–61]
years. Of the 241 patients, 96 were admitted for pneumonia, 65
for ARDS, 23 for sepsis/septic shock, 21 for trauma, 13 for cardio-
 A. Bruni et al. / Intensive & Critical Care Nursing xxx (xxxx) xxx 3

Fig. 1. Flow Diagram. Flow diagram of studies screening and selection according to the Preferred Reporting Items for Systematic review and Meta-Analysis (PRISMA)
recommendations.

Fig. 2. Risk of bias assessment. The risk of bias has been assessed for all included studies. All studies suffer of a high (red) or intermediate (white) risk for considered biases.
One only study shows a low (green) risk of selection bias. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this
article.)

genic shock and 23 for other miscellaneous reasons. All studies but
one (Lucchini et al., 2017) reported the gender; 149 patients were
males and 67 females. Three studies did not report any severity
score at ICU admission (Lucchini et al., 2017, Saez dela Fuente
et al., 2016, Sams et al., 2012). One study reported the average
APACHE score, i.e. 25.5 (8.98) (van der Voort and Zandstra, 2001),
one study the Simplified Acute Physiology Score II (SAPS-II), i.e.
52 (14) and 52 (30) in the two groups of randomised patients
(Reignier et al., 2004) and one study both SAPS-II (i.e. 52 (15)
and 55 (16) in the two studied population) and the Sequential
Organ Failure Assessment (SOFA) score, (10 (3) and 9 (4), respec-
tively) (Reignier et al., 2010).
Studies protocols
Van der Voort and Zandstra prospectively assessed the toler-
ance of EN during prone position, as compared to supine position.
EN was initiated within 24 hours of admission, at an increasing
rate up to 80ml/hour. All patients were studied for 6 hours in the
prone position and 6 hours in the supine position, with a 30° head
elevation in both positions (van der Voort and Zandstra, 2001).
Reignier and colleagues prospectively assessed the tolerance of
EN during prone position in 71 patients with severe hypoxemic
Acute Respiratory Failure. EN was started at 30ml/hour and daily
increased by 30ml/hour, in order to administer 500ml of feeding

Please cite this article as: A. Bruni, E. Garofalo, L. Grande et al., Nursing issues in enteral nutrition during prone position in critically ill patients: A system-
atic review of the literature, Intensive & Critical Care Nursing, https://doi.org/10.1016/j.iccn.2020.102899
4 A. Bruni et al. / Intensive & Critical Care Nursing xxx (xxxx) xxx

Table 1
Characteristics of included studies.

Study characteristics Population characteristics

Study Design Single- Country Sample Inclusion criteria Exclusion criteria Intervention
centre size
van der Voort and Prospective Yes The 19 Mechanical ventilation, prone Not reported Prone vs. supine
Zandstra (2001) cross-over position, PaO2/FiO2 <100 position
mmHg or pneumonia with
large amount of secretions
Reignier et al. (2004) Prospective Yes 71 Mechanical ventilation, prone Prokinetics agents 48 h before Prone vs. supine
cohort position, early EN via NG tube inclusion, gastro-intestinal position
for > 5 days bleeding or surgery, pregnancy,
facial trauma, oesophageal varices
Reignier et al. (2010) Prospective Yes 72 Mechanical ventilation, prone Prokinetics agents 48 h before 24h vs. 18h EN protocol
parallel with position, early EN via NG tube inclusion, gastro-intestinal
historical for > 5 days bleeding or surgery, pregnancy,
group facial trauma, oesophageal varices
Sams et al. (2012) Prospective Yes 20 Mechanical ventilation, prone Not reported Early EN via NG tube
parallel position, early EN tolerance vs. PP tube
randomized
Saez de la Fuente Prospective Yes 34 Mechanical ventilation, prone No exclusion criteria Prone vs. supine
et al. (2016) cross-over position, PaO2/FiO2 <150 position
mmHg, early EN
Lucchini et al. (2017) Retrospective Yes 25 Mechanical ventilation, prone Not reported Prone vs. supine
position position

PaO2/FiO2, oxygen arterial partial pressure to oxygen inspired fraction ratio; EN, enteral nut.

on the first day, 1000ml on the second, 1500ml on the third and
2000ml on the fourth and fifth days. EN was continuously deliv-
ered from 6pm to noon, while no discontinuation was applied in
patients treated with insulin (Reignier et al., 2004).
Another studied by Reignier (Reignier et al., 2010) compared
two different strategies to provide early EN in patients in prone
position. This before-after study compared a strategy (control
group) previously described (see above) (Reignier et al., 2004),
with a new protocol consisting of EN delivery over 24 hours, start-
ing at 25ml/hour and increased by 25ml/hour every 6 hours up to
80ml/hour, in absence of intolerance (Reignier et al., 2010).
In ARDS patients during prone positioning, Sams and colleagues
assessed if the incidence of micro-aspiration, detected by pepsin A
assay in the tracheal aspirate was reduced by the insertion of post-
pyloric tube, as opposed to nasogastric feeding tube (Sams et al.,
2012).
In 34 patients, Saez de la Fuente and colleagues assessed toler-
ance and safety (i.e. high gastric residual events, vomiting episodes
or regurgitation) of EN in prone position, as compared to the
supine position. EN was delivered over 24 hours, adjusting the rate
to gradually achieve an energy target of 25kcal/kg/day, in steps of
25% over the first four days (Saez dela Fuente et al., 2016).
Lastly, Lucchini and colleagues retrospectively compared the
gastric residual volume in 25 ARDS patients receiving EN during
supine and prone position. EN delivery rate was adjusted according
to a protocol based on the gastric residual volume checks (every
6 hours), and modifying the rate of infusion at steps of 21ml/hour
(Lucchini et al., 2017).
Residual gastric and EN volumes
Residual gastric volumes are reported by five studies (Lucchini
et al., 2017, Reignier et al., 2010, Reignier et al., 2004, Saez dela
Fuente et al., 2016, van der Voort and Zandstra, 2001). Single stud-
ies results are shown in Table 2. Van der Voort and colleagues
reported no differences of gastric residual volume between prone
and supine position after 3 and 6 hours of feeding (van der Voort
and Zandstra, 2001). On the contrary, Reignier (Reignier et al.,
2004) described a small, though significant difference in the resid-
ual gastric volume between prone and supine positions at day 1, 2
and 4; of note, the amount of enteral feeding administered during
prone position was lower, as compared to supine position (Reignier
et al., 2004). The rate of events of excessive residual gastric volume
was similar between patients’ groups in four studies (Lucchini
et al., 2017, Reignier et al., 2010, Saez dela Fuente et al., 2016,
van der Voort and Zandstra, 2001).
In the study by Reignier (Reignier et al., 2010), the prolongation
of EN delivery over 24 hours significantly increased the daily
administered feed volume, without any impact on the gastric resi-
due. Finally, both Saez de la Fuente and colleagues and Lucchini
and colleagues did not report differences in the residual gastric
volumes between prone and supine positions (Lucchini et al.,
2017, Saez dela Fuente et al., 2016); furthermore, in the latter
study, the EN fed volume was similar between the two conditions
(Lucchini et al., 2017).
EN intolerance events
Early EN intolerance events during prone position were
reported as the need of EN discontinuation, high residual gastric
volumes, vomiting or regurgitation episodes.
The need to stop EN was reported by two studies (Lucchini
et al., 2017, Reignier et al., 2004). Reignier and colleagues reported
a higher rate of EN discontinuation during prone position (82% of
patients, with a total of 63 times of discontinuation), as opposed
to supine position (49% of patients, with a total of 42 times of dis-
continuation) (Reignier et al., 2004). In the study by Lucchini and
colleagues, EN was stopped in 9.2% of assessments during supine
position, while in 6.8% during prone position; noteworthy, only
once the suspension was attributable to an excessive residual gas-
tric volume (>500 ml) (Lucchini et al., 2017).
Four studies have reported the number of patients showing
high residual gastric volumes (Lucchini et al., 2017, Reignier
et al., 2010, Saez dela Fuente et al., 2016, van der Voort and
Zandstra, 2001). Noteworthy, the definitions of high residual vol-
umes were different among studies. Van der Voort and Zandstra
defined the residual gastric volumes as ‘‘high” when >150ml after
6 hours of nutrition (van der Voort and Zandstra, 2001), Reignier
if >250ml (Reignier et al., 2010), Lucchini if >300ml (Lucchini
et al., 2017) and Saez de la Fuente if >500ml (Saez dela Fuente

Please cite this article as: A. Bruni, E. Garofalo, L. Grande et al., Nursing issues in enteral nutrition during prone position in critically ill patients: A system-
atic review of the literature, Intensive & Critical Care Nursing, https://doi.org/10.1016/j.iccn.2020.102899
 A. Bruni et al. / Intensive & Critical Care Nursing xxx (xxxx) xxx 5

Table 2
Gastric residual and daily enteral feeding volumes, as reported in included studies.

van der Voort and Reignier et al. (2004) Reignier et al. (2010) Saez de la Fuente et al. Lucchini et al. (2017)
Zandstra (2001) (2016)
Prone Supine Prone Supine 24h EN 18h EN Prone Supine Prone Supine
(n=19) (n=19) (n=34) (n=37) (n=34) (n=38) (n=34) (n=34) (n=25) (n=25)
Gastric Residual
Volume (ml)
3 hours 59.7 59.9
(0–200) (0–180)
6 hours 110 95
(0–325) (10–340)
Day 1 30 10 48 55
[10–100] [0–50] * [10–90] [10–180]
Day 2 45 10 45 48
[4–152] [0–53] * [10–295] [10–200]
Day 3 20 10 53 100
[0–97] [0–70] [10–250] [10–300]
Day 4 30 13 40 75
[5–148] [0–50] * [13–138] [35–180]
Day 5 13 10 55 83
[0–100] [0–70] [13–178] [35–225]
Per day 189.2 126.6
(203.2) (132.1)
Per 4–hours 23.9 (50.2) 20.6 (18.9)
period
Enteral Feeding Volume (ml)
Day 1 536 655 394 250
[425–650] [572–700] * [300–900] [150–513]
Day 2 496 1010 1415 750
[169–656] [652–1143] * [988–1800] [444–1050]
*
Day 3 730 1125 1650 1063
[538– [828–1500] * [1330– [500–1250]
1123] 1920] *
Day 4 862 1200 1830 1240
[635– [1073–1500] [1500– [750–1600]
1016] * 2040] *
Day 5 1150 1485 1980 1225
[993– [1255–1837] [1680– [800–1500]
1200] * 2040] *
% of prescribed 92.8 (5.8) 94.1 (3.5)

EN, enteral nutrition. Data are reported as mean (SD), mean (min to max range) or median [IQR], as reported by the included studies. * indicates a statistically significant
difference between groups, as reported by the included studies.

et al., 2016). In the study by van der Voort and Zandstra, six
patients showed a residual gastric volume >150ml in both supine
and prone position, while one patient showed a high vol-
ume >150ml only during prone position (van der Voort and
Zandstra, 2001). In the study by Reignier and colleagues (2010),
intolerance to EN occurred in 71% of control patients and 63% of
intervention patients (p = 0.5). Furthermore, the presence of high
residual volume was similar between intervention (58%) and con-
trol (59%) groups (p = 0.6) (Reignier et al., 2010). Lucchini reported
that only one patient (4%) suffered of high gastric residual volume
during both supine and prone positions (Lucchini et al., 2017).
Finally, Saez de la Fuente and colleagues did not report differences
in the number of high gastric residual events per day between
supine and prone positions (0.06 vs. 0.09; p=0.39) (Saez dela
Fuente et al., 2016).
Vomiting or regurgitation events were reported by four studies
(Reignier et al., 2010, Reignier et al., 2004, Saez dela Fuente et al.,
2016, van der Voort and Zandstra, 2001). Van der Voort and Zand-
stra reported only one (5%) patient vomiting during prone posi-
tioning, while none during supine. Reignier and colleagues
(2004) reported an increased risk for vomiting during prone posi-
tion (p<0.001; relative risk, 2.5; 95% confidence interval, 1.5–4.0).
In particular, 30 episodes of vomiting were reported during the
218 periods of the prone position, while 26 episodes during the
462 supine position periods (Reignier et al., 2004). In another study
by Reignier (Reignier et al., 2010), vomiting occurred in all patients
receiving the 18-hour feeding protocol, while in 9 out of 12
patients receiving 24-hour feeding protocol (Reignier et al.,
2010). In addition, Saez de la Fuente and colleagues reported no
differences between supine and prone positions with regard to
vomiting (0.016 vs 0.03; p=0.53) and diet regurgitation events
per day (0 vs 0.04; p=0.051) (Saez dela Fuente et al., 2016). Finally,
Sams and colleagues showed that the insertion of post-pyloric
feeding tube may provide a slight, though not significant, protec-
tive effect for aspiration risk in prone position, when compared
to nasogastric feed (odds ratio 0.778; 95% confidence interval:
0.09–6.98) (Sams et al., 2012).
Major clinical outcomes
Only the two studies by Reignier and colleagues assessed some
clinical outcomes between treatments (Reignier et al., 2010,
Reignier et al., 2004). In the first trial, the rate of ventilator-
associated pneumonia was similar between supine (24%) and
prone position (35%) (Reignier et al., 2004). Mortality was also sim-
ilar between groups (24% vs. 35%, respectively) (Reignier et al.,
2004).
In the second trial (Reignier et al., 2010), 10 (29%) controls and 9
(24%) interventional patients developed a ventilator-associated
pneumonia (p=0.58). The incidence of ventilator-associated pneu-
monia was 2.4 episodes every 100 patient-days of intubation in
controls, while 1.6 episodes in the intervention group. Further-

Please cite this article as: A. Bruni, E. Garofalo, L. Grande et al., Nursing issues in enteral nutrition during prone position in critically ill patients: A system-
atic review of the literature, Intensive & Critical Care Nursing, https://doi.org/10.1016/j.iccn.2020.102899
6 A. Bruni et al. / Intensive & Critical Care Nursing xxx (xxxx) xxx

more, secondary infections (such as urinary tract infections, bac-
teremia, catheter-related blood stream infections) occurred in 16
(47%) patients in the control group and 16 (42%) in the intervention
group (p = 0.81). Reignier and colleagues did not find difference
with respect to ICU length of stay (20 (13) in the control vs. 23
(13) days in the interventional group; p=0.56), and hospital length
of stay (28 (21) in control vs. 34 (29) days in the interventional
group; p=0.31). Finally, patients in the interventional group had
significantly lower rates of ICU (28%) and hospital (29%) mortality,
compared to the control group (53%, p=0.04 and 29%, p=0.009,
respectively) (Reignier et al., 2010).
residual volumes and adjustment of the rate of enteral feeding is
fundamental to increase EN tolerance (Lucchini et al., 2017).
In this scenario, intensive care nurses should be aware of the
higher risk for regurgitation and vomiting during prone position
(Reignier et al., 2004); therefore, they should be properly trained
to keep the patient with head-of-bed elevation (Reignier et al.,
2010), to monitor enteral feeding and to detect the potential signs
of EN intolerance (Lucchini et al., 2017, Reignier et al., 2010). The
presence of a predefined protocol for EN management should be
implemented to guide nurses in their daily activity, to administer
higher enteral feeding volumes and to avoid EN stop, regurgitation
or vomiting episodes (Reignier et al., 2010).

Discussion
Study limitations

The current literature on administration of EN during prone

Although this systematic review is contemporary, it suffers
position is scanty. Despite the low number of studies, administra-
from some important limitations. First of all, there is a clear lack
tion of EN during prone positioning seems to not increase the gas-
of prospective randomised controlled trials, properly designed to
tric residual volumes to a clinically relevant extent (Lucchini et al.,
assess differences in major clinical outcome (such as infections,
2017, Reignier et al., 2010, Reignier et al., 2004, Saez dela Fuente
lengths of stay, mortality). Furthermore, the heterogeneity of study
et al., 2016, van der Voort and Zandstra, 2001), although only
designs, outcomes definition and assessment, together with a low
one study reported an increased need to stop EN and rate of vom-
yield of the literature search, preclude quantitative assessment of
iting in prone position (Reignier et al., 2004). On the contrary, other
pooled study results. In addition, the quality of the included stud-
studies did not report any increased risk for regurgitation, vomit-
ies is quite low, mainly due to the retrospective or before-after
ing or pneumonia during prone position (Reignier et al., 2010,
design. Finally, we could not provide data regarding the real-life
Saez dela Fuente et al., 2016, van der Voort and Zandstra, 2001).
use of EN during prone position, due to the lack of targeted obser-
Furthermore, protocols including strategies to increase the EN tol-
vational studies. Therefore, it is desirable that future prospective
erance (head-of-bed elevation, use of prokinetic agents, continuous
and randomised studies will evaluate: 1) the real use of EN during
administration over 24 hours) may be effective to augment the
prone position, 2) the development of a properly designed protocol
feeding volume in patients during prone position (Reignier et al.,
to deliver, monitor and guide nurses in EN administration during
2010). Finally, the rate of ventilator associated pneumonia was
prone position; 3) the incidence of complications or EN intolerance
similar between patients receiving EN during supine or prone posi-
events during prone position; 4) if the early administration of EN
tion (Reignier et al., 2004).
during prone position may improve major clinical outcomes of
The recent ESICM guidelines suggest that early EN should be
patients. All of the above is important to confirm the safety and tol-
preferred to delayed EN, because it reduces the risk of infection
erability of EN during prone position, and to provide solid evidence
(Reintam Blaser et al., 2017). Furthermore, early EN: 1) should be
and strong recommendations in future guidelines.
preferred to early parenteral nutrition, 2) should be started at
low doses as soon as the shock is controlled with fluids and vaso-
pressors/inotropes, 3) should be administered in patients with con- Conclusion
trolled hypoxaemia and compensated or permissive hypercapnia
and acidosis and 4) should be assured also in case of deep sedation Although the literature is poor and scanty, EN during prone
and infusion of neuromuscular blocking agents (Reintam Blaser positioning is currently recommended by the guidelines. Both the
et al., 2017). In keeping with the ESICM guidelines (Reintam medical and nurse staff should follow protocols in order to increase
Blaser et al., 2017), the recent ESPEN guidelines strongly suggest the enteral feeding volume, while avoiding EN intolerance (such as
that early EN should also be performed in patients managed in EN stops, high residual volume, regurgitation and vomiting). The
the prone position (Singer et al., 2019). literature currently lacks of definitive data from randomised con-
Based on the evidence from the literature and, finally, on the trolled trials designed to assess if the administration of early EN
indications from guidelines (Reintam Blaser et al., 2017) (Singer during prone position may influence major clinical outcomes.
et al., 2019), there is a growing role for early EN even during prone
positioning in ARDS patients. Of note, when applied in the early Declaration of Competing Interest
phase of moderate to severe ARDS, prolonged (>16 hours) prone
positioning sessions halved the 28-day mortality (Guerin et al., The authors declare that they have no known competing finan-
2013). However, gastric emptying is delayed in up to 60% of criti- cial interests or personal relationships that could have appeared
cally ill patients; this is particularly true in patients during prone to influence the work reported in this paper.
position, with increased risk for EN intolerance, regurgitation or
vomiting (Linn et al., 2015). In this systematic review, only one
Appendix A. Supplementary data
study has reported an increased risk for EN intolerance and vomit-
ing, deeming necessary to stop EN (Reignier et al., 2004). In the
Supplementary data to this article can be found online at
case medical or nursing staff face with EN intolerance, some cor-
https://doi.org/10.1016/j.iccn.2020.102899.
rective and preventive actions can be implemented. For instance,
the use of different and predefined nutritional protocols, including
the use of prokinetics agents, post-pyloric feeding, head-of-bed References
elevation and continuous administration over 24 hours, may
Artinian, V., Krayem, H., DiGiovine, B., 2006. Effects of early enteral feeding on the
increase EN tolerance during prone position (Reignier et al., 2010, outcome of critically ill mechanically ventilated medical patients. Chest 129,
Sams et al., 2012). Furthermore, a closed monitoring of gastric 960–967.

Please cite this article as: A. Bruni, E. Garofalo, L. Grande et al., Nursing issues in enteral nutrition during prone position in critically ill patients: A system-
atic review of the literature, Intensive & Critical Care Nursing, https://doi.org/10.1016/j.iccn.2020.102899
 A. Bruni et al. / Intensive & Critical Care Nursing xxx (xxxx) xxx 7

Ding, H., Hu, G.L., Zheng, X.Y., Chen, Q., Threapleton, D.E., Zhou, Z.H., 2015. The
method quality of cross-over studies involved in Cochrane Systematic Reviews.
PLoS ONE 10, e0120519.
Guerin, C., Reignier, J., Richard, J.C., Beuret, P., Gacouin, A., Boulain, T., et al., 2013.
Prone positioning in severe acute respiratory distress syndrome. N. Engl. J. Med.
368, 2159–2168.
Liberati, A., Altman, D.G., Tetzlaff, J., Mulrow, C., Gotzsche, P.C., Ioannidis, J.P., et al.,
2009. The PRISMA statement for reporting systematic reviews and meta-
analyses of studies that evaluate health care interventions: explanation and
elaboration. J. Clin. Epidemiol. 62, e1–e34.
Linn, D.D., Beckett, R.D., Foellinger, K., 2015. Administration of enteral nutrition to
adult patients in the prone position. Intensive Crit. Care Nurs. 31, 38–43.
Lucchini, A., Bonetti, I., Borrelli, G., Calabrese, N., Volpe, S., Gariboldi, R., et al., 2017.
[Enteral nutrition during prone positioning in mechanically ventilated
patients]. Assist Inferm. Ric. 36, 76–83.
Lucchini, A., De Felippis, C., Pelucchi, G., Grasselli, G., Patroniti, N., Castagna, L., et al.,
2018. Application of prone position in hypoxaemic patients supported by veno-
venous ECMO. Intensive Crit. Care Nurs. 48, 61–68.
Marik, P.E., Zaloga, G.P., 2001. Early enteral nutrition in acutely ill patients: a
systematic review. Crit. Care Med. 29, 2264–2270.
Messina, A., Longhini, F., Coppo, C., Pagni, A., Lungu, R., Ronco, C., et al., 2017. Use of
the fluid challenge in critically ill adult patients: a systematic review. Anesth.
Analg. 125, 1532–1543.
Messina, A., Pelaia, C., Bruni, A., Garofalo, E., Bonicolini, E., Longhini, F., et al., 2018.
Fluid challenge during anesthesia: a systematic review and meta-analysis.
Anesth. Analg. 127, 1353–1364.
Piehl, M.A., Brown, R.S., 1976. Use of extreme position changes in acute respiratory
failure. Crit. Care Med. 4, 13–14.
Reignier, J., Dimet, J., Martin-Lefevre, L., Bontemps, F., Fiancette, M., Clementi, E.,
et al., 2010. Before-after study of a standardized ICU protocol for early
enteral feeding in patients turned in the prone position. Clin Nutr. 29, 210–
216.
Reignier, J., Thenoz-Jost, N., Fiancette, M., Legendre, E., Lebert, C., Bontemps, F., et al.,
2004. Early enteral nutrition in mechanically ventilated patients in the prone
position. Crit. Care Med. 32, 94–99.
Reintam Blaser, A., Starkopf, J., Alhazzani, W., Berger, M.M., Casaer, M.P., Deane, A.
M., et al., 2017. Early enteral nutrition in critically ill patients: ESICM clinical
practice guidelines. Intensive Care Med. 43, 380–398.
Saez de la Fuente, I., Saez de la Fuente, J., Quintana Estelles, M.D., Garcia Gigorro, R.,
Terceros Almanza, L.J., Sanchez Izquierdo, J.A., et al., 2016. Enteral nutrition in
patients receiving mechanical ventilation in a prone position. JPEN J. Parenter.
Enteral. Nutr. 40, 250–255.
Sams, V.G., Lawson, C.M., Humphrey, C.L., Brantley, S.L., Schumacher, L.M., Karlstad,
M.D., et al., 2012. Effect of rotational therapy on aspiration risk of enteral feeds.
Nutr. Clin. Pract. 27, 808–811.
Singer, P., Blaser, A.R., Berger, M.M., Alhazzani, W., Calder, P.C., Casaer, M.P., et al.,
2019. ESPEN guideline on clinical nutrition in the intensive care unit. Clin. Nutr.
38, 48–79.
van der Voort, P.H., Zandstra, D.F., 2001. Enteral feeding in the critically ill:
comparison between the supine and prone positions: a prospective crossover
study in mechanically ventilated patients. Crit. Care 5, 216–220.

Please cite this article as: A. Bruni, E. Garofalo, L. Grande et al., Nursing issues in enteral nutrition during prone position in critically ill patients: A system-
atic review of the literature, Intensive & Critical Care Nursing, https://doi.org/10.1016/j.iccn.2020.102899