Annika Reintam Blaser
Manu L. N. G. Malbrain
Joel Starkopf
Sonja Fruhwald
Stephan M. Jakob
Jan De Waele
Jan-Peter Braun
Martijn Poeze
Claudia Spies
Gastrointestinal function in intensive care
patients: terminology, definitions
and management. Recommendations
of the ESICM Working Group on Abdominal
Problems
Received: 27 June 2011
Accepted: 20 December 2011
Published online: 7 February 2012
� The Author(s) 2012. This article is
published with open access at
Springerlink.com
On behalf of the Working Group on
Abdominal Problems of the European
Society of Intensive Care Medicine (ESICM
WGAP).
Electronic supplementary material
The online version of this article
(doi:10.1007/s00134-011-2459-y) contains
supplementary material, which is available
to authorized users.
A. Reintam Blaser ()) � J. Starkopf
Clinic of Anaesthesiology and Intensive
Care, University of Tartu, Puusepa 8,
51014 Tartu, Estonia
e-mail: annika.reintam@ut.ee;
annika.reintam.blaser@ut.ee
Tel.: ?372-5-142281
Fax: ?372-5-3318406
A. Reintam Blaser � S. M. Jakob
Department of Intensive Care Medicine,
University Hospital (Inselspital) and
University of Bern, 3010 Bern, Switzerland
M. L. N. G. Malbrain
Intensive Care Unit, Ziekenhuis Netwerk
Antwerpen, ZNA Stuivenberg,
Lange Beeldekensstraat 267,
2060 Antwerpen, Belgium
J. Starkopf
Clinic of Anaesthesiology and Intensive
Care, Tartu University Hospital,
Puusepa 8, 51014 Tartu, Estonia
S. Fruhwald
Department of Anaesthesiology and
Intensive Care Medicine, Medical
University of Graz, Auenbruggerplatz 29,
8036 Graz, Austria
J. De Waele
Department of Critical Care Medicine,
Ghent University Hospital and Ghent
Medical School, De Pintelaan 185,
9000 Ghent, Belgium
J.-P. Braun � C. Spies
Department of Anaesthesiology
and Intensive Care,
Charite´, Universita¨tsmedizin Berlin,
Charite´platz 1, 10117 Berlin, Germany
M. Poeze
Division of Traumatology,
Department of Surgery, Maastricht
University Medical Center, P. Debyelaan
25, 6202 AZ Maastricht, The Netherlands
Abstract Purpose: Acute gastro-
intestinal (GI) dysfunction and failure
have been increasingly recognized in
critically ill patients. The variety of
definitions proposed in the past has
led to confusion and difficulty in
comparing one study to another. An
international working group con-
vened to standardize the definitions
for acute GI failure and GI symptoms
and to review the therapeutic options.
Methods: The Working Group on
Abdominal Problems (WGAP) of the
European Society of Intensive Care
Medicine (ESICM) developed the
definitions for GI dysfunction in
intensive care patients on the basis of
the available evidence and current
understanding of the pathophysiol-
ogy. Results: Definitions for acute
gastrointestinal injury (AGI) with its
four grades of severity, as well as for
feeding intolerance syndrome and GI
symptoms (e.g. vomiting, diarrhoea,
paralysis, high gastric residual vol-
umes) are proposed. AGI is a
malfunctioning of the GI tract in
intensive care patients due to their
acute illness. AGI grade
I = increased risk of developing GI
dysfunction or failure (a self-limiting
condition); AGI grade II = GI dys-
function (a condition that requires
interventions); AGI grade III = GI
failure (GI function cannot be
restored with interventions); AGI
grade IV = dramatically manifesting
GI failure (a condition that is imme-
diately life-threatening). Current
evidence and expert opinions regard-
ing treatment of acute GI dysfunction
are provided. Conclusions: State-of-
the-art definitions for GI dysfunction
with gradation as well as management
recommendations are proposed on the
basis of current medical evidence and
expert opinion. The WGAP recom-
mends using these definitions for
clinical and research purposes.
Key
s Gastrointestinal function �
Failure � Symptoms � Feeding
intolerance � Intensive care �
Definitions � Classification
Intensive Care Med (2012) 38:384–394
DOI 10.1007/s00134-011-2459-y CONFERENCE REPORTS AND EXPERT PANEL
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Introduction
More than 10 years ago a round-table conference on gut
dysfunction in critical illness concluded that intestinal
function is an important determinant in the outcome of
patients admitted to the intensive care unit (ICU), but that
there is no objective and clinically relevant definition of
gastrointestinal (GI) dysfunction in critical illness. In
addition, it was stated that the definition developed in the
future should grade the severity of dysfunction [1].
The problems in defining GI dysfunction start with
defining GI function. Next to the digestive tract, the GI
tract also carries out endocrine, immune and barrier
functions. The clinical assessment of the impairment of
these functions today is more intuitive than objective.
Therefore, endocrine, immune and barrier dysfunctions
will not be addressed in detail in the present paper.
Several studies have confirmed that GI symptoms are
frequent in the ICU with up to 62% of patients exhibiting at
least one GI symptom for at least 1 day [2–4]. There is also
increasing evidence that development of GI problems is
related to worse outcome in critically ill patients [2, 5–7].
Different definitions for separate GI symptoms have
been used. The lack of markers for the measurement of GI
function has suppressed studies in this field as well as the
assessment of GI dysfunction as an organ failure.
Although plasma citrulline and intestinal fatty acid
binding protein have been proposed as possible markers
for small bowel function [8], their clinical use in diag-
nosis and management of GI dysfunction is still unclear.
At least partly due to the lack of a formal definition
and classification, treatment strategies for GI problems
have been difficult to develop and are currently based on
experience, rather than evidence.
There is increasing evidence that early protocolized
and goal-oriented care can improve organ function and
the patients’ outcome during critical illness [9–12].
Improving the definition of GI dysfunction as a part of the
multiple organ dysfunction syndrome (MODS) and its
derived sequential organ failure assessment score (SOFA)
[13] will establish the base for setting up the bundle of
preventive and therapeutic measures and support the
development of novel treatment strategies.
For these reasons, the Working Group on Abdominal
Problems (WGAP) as part of the Perioperative Intensive
Care (POIC) section of the European Society of Intensive
Care Medicine (ESICM) proposes a set of definitions and
grading system of GI dysfunction in critical illness that
are applicable both for clinical and research purposes.
Methods
Several key elements were used as a starting point for
defining acute GI organ failure. An organ failure was
considered as a dichotomous event that is either present or
absent, whereas organ dysfunction is a continuum of
physiologic derangement [14]. The expression ‘‘GI dys-
function’’ is used to describe the large variety of GI
symptoms (diarrhoea, vomiting) and diagnoses (gastro-
enteritis) outside of the ICU setting; therefore, the
expression ‘‘acute GI injury’’ was introduced.
Current definitions and management recommendations
(according to Table 1; [15]) were developed on the basis
of the available evidence and current understanding of the
pathophysiology. Definitions serve as expert opinion, with
their reasoning given in each ‘‘rationale’’ subsection.
The working method is described in detail in the
electronic supplementary file.
Results
The WGAP suggests using the following terminology and
definitions:
1. Gastrointestinal function
The human GI tract has many functions including
facilitating digestion to absorb nutrients and water,
barrier control to modulate absorption of intraluminal
microbes (and their products), endocrine and immune
functions. Perfusion, secretion, motility and a coordi-
nated gut–microbiome interaction are prerequisites for
an adequate function [16].
It needs to be underlined that because we currently
lack the tool or marker to measure GI function we
cannot reliably decide about normal GI function in the
acute setting.
2. Acute gastrointestinal injury (AGI) and its different
grades
Acute GI injury (AGI) is malfunctioning of the GI
tract in critically ill patients due to their acute illness.
According to severity the following grades of AGI can
be distinguished:
Table 1 Grading of the quality of evidence and strength of
recommendations
Quality of evidence Rationale
A High RCT or meta-analyses
B Moderate Downgraded RCTs or upgraded
observational studies
C Low Well-done observational studies
D Very low Case series or expert opinion
Strength of recommendation
Grade 1 Strong We recommend
Grade 2 Weak We suggest
RCT randomized controlled trial
385
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2.1 AGI grade I (risk of developing GI dysfunction or
failure)—the function of the GI tract is partially
impaired, expressed as GI symptoms related to a
known cause and perceived as transient.
Rationale Condition is clinically seen as occur-
rence of GI symptoms after an insult, which
expectedly has temporary and self-limiting
nature.
Examples Postoperative nausea and/or vomiting
during the first days after abdominal surgery,
postoperative absence of bowel sounds, dimin-
ished bowel motility in the early phase of
shock.
Management The general condition is usually
improving and specific interventions for GI
symptoms are not needed, except the replace-
ment of fluid requirements by intravenous
infusions. Early enteral feeding, started within
24–48 h after the injury, is recommended [17,
18] (grade 1B). The use of drugs impairing GI
motility (e.g. catecholamines, opioids) has to be
limited whenever possible [19–22] (grade 1C).
2.2 AGI grade II (gastrointestinal dysfunction)—the GI
tract is not able to perform digestion and
absorption adequately to satisfy the nutrient
and fluid requirements of the body. There are
no changes in general condition of the patient
related to GI problems.
Rationale The condition is characterized by
acute occurrence of GI symptoms requiring
therapeutic interventions for achievement of
nutrient and fluid requirements. This condition
occurs without previous GI interventions or is
more severe than might be expected in relation to
the course of preceding abdominal procedures.
Examples Gastroparesis with high gastric resid-
uals or reflux, paralysis of the lower GI tract,
diarrhoea, intra-abdominal hypertension (IAH)
grade I (intra-abdominal pressure (IAP)
12–15 mmHg), visible blood in gastric content
or stool. Feeding intolerance is present if at least
20 kcal/kg BW/day via enteral route cannot be
reached within 72 h of feeding attempt.
Management Measures to treat the condition and
to prevent the progression to GI failure need to be
undertaken (e.g. treatment of intra-abdominal
hypertension [23], grade 1D; or measures to
restore the motility function of GI tract, such as
prokinetic therapy [24–26], grade 1C). Enteral
feeding should be started or continued; in cases of
high gastric residuals/reflux or feeding intoler-
ance regular challenges with small amounts of
enteral nutrition (EN) should be regularly con-
sidered (grade 2D). In patients with gastroparesis,
initiation of postpyloric feeding should be
considered in this state, when prokinetic therapy
is not effective (grade 2D).
2.3 AGI grade III (gastrointestinal failure)—loss of GI
function, where restoration of GI function is not
achieved despite interventions and the general
condition is not improving.
Rationale Clinically seen as sustained intoler-
ance to enteral feeding without improvement
after treatment (e.g. erythromycin, postpyloric
tube placement), leading to persistence or wors-
ening of MODS.
Examples Despite treatment, feeding intolerance
is persisting—high gastric residuals, persisting
GI paralysis, occurrence or worsening of bowel
dilatation, progression of IAH to grade II (IAP
15–20 mmHg), low abdominal perfusion pres-
sure (APP) (below 60 mmHg). Feeding
intolerance is present and possibly associated
with persistence or worsening of MODS.
Management Measures to prevent worsening of
GI failure are warranted (e.g. monitoring and
targeted treatment of IAH [23], grade 1D).
Presence of undiagnosed abdominal problem
(cholecystitis, peritonitis, bowel ischaemia)
should be excluded. The medications promoting
GI paralysis have to be discontinued as far as
possible [19–22] (grade 1C). Early parenteral
feeding (within the first 7 days of ICU stay)
supplementary to insufficient enteral nutrition is
associated with higher incidence of hospital
infections and should be avoided [27] (grade
2B). Challenges with small amounts of EN
should be regularly considered (grade 2D).
2.4 AGI grade IV (gastrointestinal failure with severe
impact on distant organ function)—AGI has pro-
gressed to become directly and immediately life-
threatening, with worsening of MODS and shock.
Rationale Situation when AGI has led to an acute
critical deterioration of the general condition of the
patient with distant organ dysfunction(s).
Examples Bowel ischaemia with necrosis, GI
bleeding leading to haemorrhagic shock, Ogilvie’s
syndrome, abdominal compartment syndrome
(ACS) requiring decompression.
Management Condition requires laparotomy or
other emergency interventions (e.g., colonoscopy
for colonic decompression) for life-saving indica-
tions [28–30] (grade 1D). There is no proven
conservative approach to resolve this situation.
As differentiation of the acute GI problem from
previously existing chronic condition might be very
difficult, we suggest using the same definitions also
in cases where the condition (e.g. GI bleeding,
diarrhoea, etc.) might be due to a chronic GI disease
386
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(e.g. Crohn’s disease). In patients on chronic
parenteral feeding, GI failure (equal to AGI III)
should be considered chronically present, and no
new acute interventions to restore function are
indicated. However, monitoring of IAH and exclu-
sion of the new acute abdominal problems should
be performed similarly as in AGI grade III
management.
2.5 Primary and secondary AGI
2.5.1 Primary AGI is associated with primary disease or
direct injury to organs of the GI system
(first hit).
Rationale Condition may usually be
observed early (during the first day) after
the insult to the GI system.
Examples Peritonitis, pancreatic or
hepatic pathology, abdominal surgery,
abdominal trauma, etc.
2.5.2 Secondary AGI develops as the consequence of a
host response in critical illness without
primary pathology in the GI system
(second hit).
Rationale Condition develops without
direct insult to the GI tract.
Examples GI malfunction in a patient
with pneumonia, cardiac pathology, non-
abdominal surgery or trauma, postresus-
citation state.
3. Feeding intolerance syndrome (FI)
FI is a general term indicating intolerance of enteral
feeding for whatever clinical reason (vomiting, high
gastric residuals, diarrhoea, GI bleeding, presence of
entero-cutaneous fistulas, etc.).
Rationale Diagnosis is based on complex clinical
evaluation. There is no single clear-cut symptom or
value that defines FI [31]. Several symptoms are
commonly present.
FI should be considered present if at least 20 kcal/
kg BW/day via enteral route cannot be reached within
72 h of feeding attempt or if enteral feeding has to be
stopped for whatever clinical reason. FI should not be
considered as present if enteral feeding is electively not
prescribed or is withheld/interrupted due to procedures.
FI in special conditions: in a patient with postpyloric
feeding, FI is defined similarly to gastric feeding. If a
patient is not fed enterally due to the presence of entero-
atmospheric fistulas, FI should be considered present. If
the patient undergoes a surgical intervention for ACS or
for changing of surgical dressings of an open abdomen,
FI should be considered present immediately after
surgery unless enteral feeding can be administered.
Management FI requires efforts to maintain/restore GI
function: limiting the use of drugs impairing motility,
application of prokinetics and/or laxatives [32–34]
(grade 1C), and controlling IAP. Challenges with
small amounts of EN should be regularly considered.
In patients not tolerating enteral feeding, supplemental
parenteral nutrition should be considered [35, 36]
(grade 2D). Recent data suggest that delay for 1 week
with parenteral nutrition enhances recovery when
compared to early intravenous feeding [27] (grade
2B).
4. Intra-abdominal hypertension (IAH)
4.1 IAH is present if IAP is found to be 12 mmHg or
higher, confirmed by at least two measurements,
1–6 h apart [37].
Rationale Normal IAP is around 5–7 mmHg [38].
There are inherent variations and fluctuations in
the IAP. IAH should also be considered present if
the mean of the IAP measurements of the day is
12 mmHg or higher provided that at least four
measurements were performed [39].
Management Monitoring of fluid resuscitation is
necessary to avoid over-resuscitation [23] (grade
1C). Continuous thoracic epidural analgesia may
decrease IAP in postoperative patients with
primary IAH [40] (grade 2B). Nasogastric/colonic
decompression is suggested for evacuation of
intraluminal contents [23] (grade 2D). In patients
with intraperitoneal fluids, percutaneous catheter
decompression is recommended [23] (grade 1C).
Elevation of head of bed above 20� should be
considered as an additional risk for development
of IAH [23] (grade 2C). Neuromuscular blockade
decreases the IAP [41], but due to many undesir-
able effects it should be considered only in
selected patients (grade 2C).
4.2 Abdominal compartment syndrome (ACS) is
defined as a sustained (minimally two standard-
ized measurements, performed 1–6 h apart)
increase in IAP above 20 mmHg with new onset
organ failure [37].
Management Although decompression remains
the only definite management for ACS, the exact
indications and timing of this procedure still
remain controversial [42]. Currently it is recom-
mended (1) to perform surgical decompression as
a life-saving intervention in patients with ACS
that is refractory to other treatment options [28,
43] (grade 1D), and (2) to consider pre-emptive
decompression at the time of laparotomy in
patients who demonstrate multiple risk factors
for IAH/ACS [23] (grade 1D). In most severe
cases of ruptured abdominal aortic aneurysm or
abdominal trauma the initial use of mesh closure
avoids development of ACS [44, 45] (grade 1C).
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5. Gastrointestinal symptoms
5.1 Vomiting (emesis) is the occurrence of any visible
regurgitation of gastric content irrespective of
the amount.
Rationale Vomiting is commonly defined as the
oral expulsion of GI contents resulting from
contractions of gut and thoracoabdominal wall
musculature [46]. Vomiting is contrasted with
regurgitation, which is the effortless passage of
gastric contents into the mouth [46]. In ICU
patients the forcefulness of the act is often not
detectable; therefore, regurgitation and vomiting
should be assessed together.
Management Several guidelines for prevention
and management of postoperat