You are on page 1of 11

Intensive Care Med (2012) 38:384394

DOI 10.1007/s00134-011-2459-y CO NFERENCE REPORTS AND EXPERT PANEL

Annika Reintam Blaser


Manu L. N. G. Malbrain
Gastrointestinal function in intensive care
Joel Starkopf patients: terminology, definitions
Sonja Fruhwald
Stephan M. Jakob and management. Recommendations
Jan De Waele
Jan-Peter Braun of the ESICM Working Group on Abdominal
Martijn Poeze
Claudia Spies
Problems

S. Fruhwald the available evidence and current


Received: 27 June 2011 Department of Anaesthesiology and
Accepted: 20 December 2011 understanding of the pathophysiol-
Intensive Care Medicine, Medical ogy. Results: Definitions for acute
Published online: 7 February 2012
The Author(s) 2012. This article is University of Graz, Auenbruggerplatz 29,
8036 Graz, Austria gastrointestinal injury (AGI) with its
published with open access at four grades of severity, as well as for
Springerlink.com
J. De Waele feeding intolerance syndrome and GI
On behalf of the Working Group on Department of Critical Care Medicine, symptoms (e.g. vomiting, diarrhoea,
Abdominal Problems of the European Ghent University Hospital and Ghent paralysis, high gastric residual vol-
Society of Intensive Care Medicine (ESICM Medical School, De Pintelaan 185,
WGAP).
umes) are proposed. AGI is a
9000 Ghent, Belgium malfunctioning of the GI tract in
Electronic supplementary material intensive care patients due to their
The online version of this article J.-P. Braun  C. Spies
acute illness. AGI grade
(doi:10.1007/s00134-011-2459-y) contains Department of Anaesthesiology
supplementary material, which is available and Intensive Care, I = increased risk of developing GI
to authorized users. Charite, Universitatsmedizin Berlin, dysfunction or failure (a self-limiting
Chariteplatz 1, 10117 Berlin, Germany condition); AGI grade II = GI dys-
function (a condition that requires
M. Poeze interventions); AGI grade III = GI
Division of Traumatology,
Department of Surgery, Maastricht failure (GI function cannot be
A. Reintam Blaser ())  J. Starkopf restored with interventions); AGI
Clinic of Anaesthesiology and Intensive University Medical Center, P. Debyelaan
Care, University of Tartu, Puusepa 8, 25, 6202 AZ Maastricht, The Netherlands grade IV = dramatically manifesting
51014 Tartu, Estonia GI failure (a condition that is imme-
e-mail: annika.reintam@ut.ee; diately life-threatening). Current
annika.reintam.blaser@ut.ee Abstract Purpose: Acute gastro- evidence and expert opinions regard-
Tel.: ?372-5-142281 intestinal (GI) dysfunction and failure ing treatment of acute GI dysfunction
Fax: ?372-5-3318406 have been increasingly recognized in are provided. Conclusions: State-of-
critically ill patients. The variety of the-art definitions for GI dysfunction
A. Reintam Blaser  S. M. Jakob definitions proposed in the past has
Department of Intensive Care Medicine, with gradation as well as management
led to confusion and difficulty in recommendations are proposed on the
University Hospital (Inselspital) and
University of Bern, 3010 Bern, Switzerland
comparing one study to another. An basis of current medical evidence and
international working group con- expert opinion. The WGAP recom-
M. L. N. G. Malbrain vened to standardize the definitions mends using these definitions for
Intensive Care Unit, Ziekenhuis Netwerk for acute GI failure and GI symptoms clinical and research purposes.
Antwerpen, ZNA Stuivenberg, and to review the therapeutic options.
Lange Beeldekensstraat 267, Methods: The Working Group on
2060 Antwerpen, Belgium Keywords Gastrointestinal function 
Abdominal Problems (WGAP) of the Failure  Symptoms  Feeding
J. Starkopf
European Society of Intensive Care intolerance  Intensive care 
Clinic of Anaesthesiology and Intensive Medicine (ESICM) developed the Definitions  Classification
Care, Tartu University Hospital, definitions for GI dysfunction in
Puusepa 8, 51014 Tartu, Estonia intensive care patients on the basis of
385

Introduction considered as a dichotomous event that is either present or


absent, whereas organ dysfunction is a continuum of
More than 10 years ago a round-table conference on gut physiologic derangement [14]. The expression GI dys-
dysfunction in critical illness concluded that intestinal function is used to describe the large variety of GI
function is an important determinant in the outcome of symptoms (diarrhoea, vomiting) and diagnoses (gastro-
patients admitted to the intensive care unit (ICU), but that enteritis) outside of the ICU setting; therefore, the
there is no objective and clinically relevant definition of expression acute GI injury was introduced.
gastrointestinal (GI) dysfunction in critical illness. In Current definitions and management recommendations
addition, it was stated that the definition developed in the (according to Table 1; [15]) were developed on the basis
future should grade the severity of dysfunction [1]. of the available evidence and current understanding of the
The problems in defining GI dysfunction start with pathophysiology. Definitions serve as expert opinion, with
defining GI function. Next to the digestive tract, the GI their reasoning given in each rationale subsection.
tract also carries out endocrine, immune and barrier The working method is described in detail in the
functions. The clinical assessment of the impairment of electronic supplementary file.
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 Results
frequent in the ICU with up to 62% of patients exhibiting at
least one GI symptom for at least 1 day [24]. There is also The WGAP suggests using the following terminology and
increasing evidence that development of GI problems is definitions:
related to worse outcome in critically ill patients [2, 57].
Different definitions for separate GI symptoms have 1. Gastrointestinal function
been used. The lack of markers for the measurement of GI The human GI tract has many functions including
function has suppressed studies in this field as well as the facilitating digestion to absorb nutrients and water,
assessment of GI dysfunction as an organ failure. barrier control to modulate absorption of intraluminal
Although plasma citrulline and intestinal fatty acid microbes (and their products), endocrine and immune
binding protein have been proposed as possible markers functions. Perfusion, secretion, motility and a coordi-
for small bowel function [8], their clinical use in diag- nated gutmicrobiome interaction are prerequisites for
nosis and management of GI dysfunction is still unclear. an adequate function [16].
At least partly due to the lack of a formal definition It needs to be underlined that because we currently
and classification, treatment strategies for GI problems lack the tool or marker to measure GI function we
have been difficult to develop and are currently based on cannot reliably decide about normal GI function in the
experience, rather than evidence. acute setting.
There is increasing evidence that early protocolized 2. Acute gastrointestinal injury (AGI) and its different
and goal-oriented care can improve organ function and grades
the patients outcome during critical illness [912]. Acute GI injury (AGI) is malfunctioning of the GI
Improving the definition of GI dysfunction as a part of the tract in critically ill patients due to their acute illness.
multiple organ dysfunction syndrome (MODS) and its According to severity the following grades of AGI can
derived sequential organ failure assessment score (SOFA) be distinguished:
[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 Table 1 Grading of the quality of evidence and strength of
recommendations
Care (POIC) section of the European Society of Intensive
Care Medicine (ESICM) proposes a set of definitions and Quality of evidence Rationale
grading system of GI dysfunction in critical illness that
are applicable both for clinical and research purposes. 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
Methods Strength of recommendation
Grade 1 Strong We recommend
Grade 2 Weak We suggest
Several key elements were used as a starting point for
defining acute GI organ failure. An organ failure was RCT randomized controlled trial
386

2.1 AGI grade I (risk of developing GI dysfunction or considered in this state, when prokinetic therapy
failure)the function of the GI tract is partially is not effective (grade 2D).
impaired, expressed as GI symptoms related to a 2.3 AGI grade III (gastrointestinal failure)loss of GI
known cause and perceived as transient. function, where restoration of GI function is not
Rationale Condition is clinically seen as occur- achieved despite interventions and the general
rence of GI symptoms after an insult, which condition is not improving.
expectedly has temporary and self-limiting Rationale Clinically seen as sustained intoler-
nature. ance to enteral feeding without improvement
Examples Postoperative nausea and/or vomiting after treatment (e.g. erythromycin, postpyloric
during the first days after abdominal surgery, tube placement), leading to persistence or wors-
postoperative absence of bowel sounds, dimin- ening of MODS.
ished bowel motility in the early phase of Examples Despite treatment, feeding intolerance
shock. is persistinghigh gastric residuals, persisting
Management The general condition is usually GI paralysis, occurrence or worsening of bowel
improving and specific interventions for GI dilatation, progression of IAH to grade II (IAP
symptoms are not needed, except the replace- 1520 mmHg), low abdominal perfusion pres-
ment of fluid requirements by intravenous sure (APP) (below 60 mmHg). Feeding
infusions. Early enteral feeding, started within intolerance is present and possibly associated
2448 h after the injury, is recommended [17, with persistence or worsening of MODS.
18] (grade 1B). The use of drugs impairing GI Management Measures to prevent worsening of
motility (e.g. catecholamines, opioids) has to be GI failure are warranted (e.g. monitoring and
limited whenever possible [1922] (grade 1C). targeted treatment of IAH [23], grade 1D).
2.2 AGI grade II (gastrointestinal dysfunction)the GI Presence of undiagnosed abdominal problem
tract is not able to perform digestion and (cholecystitis, peritonitis, bowel ischaemia)
absorption adequately to satisfy the nutrient should be excluded. The medications promoting
and fluid requirements of the body. There are GI paralysis have to be discontinued as far as
no changes in general condition of the patient possible [1922] (grade 1C). Early parenteral
related to GI problems. feeding (within the first 7 days of ICU stay)
Rationale The condition is characterized by supplementary to insufficient enteral nutrition is
acute occurrence of GI symptoms requiring associated with higher incidence of hospital
therapeutic interventions for achievement of infections and should be avoided [27] (grade
nutrient and fluid requirements. This condition 2B). Challenges with small amounts of EN
occurs without previous GI interventions or is should be regularly considered (grade 2D).
more severe than might be expected in relation to 2.4 AGI grade IV (gastrointestinal failure with severe
the course of preceding abdominal procedures. impact on distant organ function)AGI has pro-
Examples Gastroparesis with high gastric resid- gressed to become directly and immediately life-
uals or reflux, paralysis of the lower GI tract, threatening, with worsening of MODS and shock.
diarrhoea, intra-abdominal hypertension (IAH) Rationale Situation when AGI has led to an acute
grade I (intra-abdominal pressure (IAP) critical deterioration of the general condition of the
1215 mmHg), visible blood in gastric content patient with distant organ dysfunction(s).
or stool. Feeding intolerance is present if at least Examples Bowel ischaemia with necrosis, GI
20 kcal/kg BW/day via enteral route cannot be bleeding leading to haemorrhagic shock, Ogilvies
reached within 72 h of feeding attempt. syndrome, abdominal compartment syndrome
Management Measures to treat the condition and (ACS) requiring decompression.
to prevent the progression to GI failure need to be Management Condition requires laparotomy or
undertaken (e.g. treatment of intra-abdominal other emergency interventions (e.g., colonoscopy
hypertension [23], grade 1D; or measures to for colonic decompression) for life-saving indica-
restore the motility function of GI tract, such as tions [2830] (grade 1D). There is no proven
prokinetic therapy [2426], grade 1C). Enteral conservative approach to resolve this situation.
feeding should be started or continued; in cases of
high gastric residuals/reflux or feeding intoler- As differentiation of the acute GI problem from
ance regular challenges with small amounts of previously existing chronic condition might be very
enteral nutrition (EN) should be regularly con- difficult, we suggest using the same definitions also
sidered (grade 2D). In patients with gastroparesis, in cases where the condition (e.g. GI bleeding,
initiation of postpyloric feeding should be diarrhoea, etc.) might be due to a chronic GI disease
387

(e.g. Crohns disease). In patients on chronic application of prokinetics and/or laxatives [3234]
parenteral feeding, GI failure (equal to AGI III) (grade 1C), and controlling IAP. Challenges with
should be considered chronically present, and no small amounts of EN should be regularly considered.
new acute interventions to restore function are In patients not tolerating enteral feeding, supplemental
indicated. However, monitoring of IAH and exclu- parenteral nutrition should be considered [35, 36]
sion of the new acute abdominal problems should (grade 2D). Recent data suggest that delay for 1 week
be performed similarly as in AGI grade III with parenteral nutrition enhances recovery when
management. compared to early intravenous feeding [27] (grade
2B).
2.5 Primary and secondary AGI
4. Intra-abdominal hypertension (IAH)

2.5.1 Primary AGI is associated with primary disease or


direct injury to organs of the GI system 4.1 IAH is present if IAP is found to be 12 mmHg or
(first hit). higher, confirmed by at least two measurements,
Rationale Condition may usually be 16 h apart [37].
observed early (during the first day) after Rationale Normal IAP is around 57 mmHg [38].
the insult to the GI system. There are inherent variations and fluctuations in
Examples Peritonitis, pancreatic or the IAP. IAH should also be considered present if
hepatic pathology, abdominal surgery, the mean of the IAP measurements of the day is
abdominal trauma, etc. 12 mmHg or higher provided that at least four
2.5.2 Secondary AGI develops as the consequence of a measurements were performed [39].
host response in critical illness without Management Monitoring of fluid resuscitation is
primary pathology in the GI system necessary to avoid over-resuscitation [23] (grade
(second hit). 1C). Continuous thoracic epidural analgesia may
Rationale Condition develops without decrease IAP in postoperative patients with
direct insult to the GI tract. primary IAH [40] (grade 2B). Nasogastric/colonic
Examples GI malfunction in a patient decompression is suggested for evacuation of
with pneumonia, cardiac pathology, non- intraluminal contents [23] (grade 2D). In patients
abdominal surgery or trauma, postresus- with intraperitoneal fluids, percutaneous catheter
citation state. decompression is recommended [23] (grade 1C).
3. Feeding intolerance syndrome (FI) Elevation of head of bed above 20 should be
FI is a general term indicating intolerance of enteral considered as an additional risk for development
feeding for whatever clinical reason (vomiting, high of IAH [23] (grade 2C). Neuromuscular blockade
gastric residuals, diarrhoea, GI bleeding, presence of decreases the IAP [41], but due to many undesir-
entero-cutaneous fistulas, etc.). able effects it should be considered only in
Rationale Diagnosis is based on complex clinical selected patients (grade 2C).
evaluation. There is no single clear-cut symptom or 4.2 Abdominal compartment syndrome (ACS) is
value that defines FI [31]. Several symptoms are defined as a sustained (minimally two standard-
commonly present. ized measurements, performed 16 h apart)
FI should be considered present if at least 20 kcal/ increase in IAP above 20 mmHg with new onset
kg BW/day via enteral route cannot be reached within organ failure [37].
72 h of feeding attempt or if enteral feeding has to be Management Although decompression remains
stopped for whatever clinical reason. FI should not be the only definite management for ACS, the exact
considered as present if enteral feeding is electively not indications and timing of this procedure still
prescribed or is withheld/interrupted due to procedures. remain controversial [42]. Currently it is recom-
FI in special conditions: in a patient with postpyloric mended (1) to perform surgical decompression as
feeding, FI is defined similarly to gastric feeding. If a a life-saving intervention in patients with ACS
patient is not fed enterally due to the presence of entero- that is refractory to other treatment options [28,
atmospheric fistulas, FI should be considered present. If 43] (grade 1D), and (2) to consider pre-emptive
the patient undergoes a surgical intervention for ACS or decompression at the time of laparotomy in
for changing of surgical dressings of an open abdomen, patients who demonstrate multiple risk factors
FI should be considered present immediately after for IAH/ACS [23] (grade 1D). In most severe
surgery unless enteral feeding can be administered. cases of ruptured abdominal aortic aneurysm or
Management FI requires efforts to maintain/restore GI abdominal trauma the initial use of mesh closure
function: limiting the use of drugs impairing motility, avoids development of ACS [44, 45] (grade 1C).
388

5. Gastrointestinal symptoms 5.3 Diarrhoea is defined as having three or more loose


or liquid stools per day with a stool weight
5.1 Vomiting (emesis) is the occurrence of any visible greater than 200250 g/day (or greater then
regurgitation of gastric content irrespective of 250 ml/day) [60, 61].
the amount. Rationale Normal bowel frequency ranges from
Rationale Vomiting is commonly defined as the three times a week to three times a day.
oral expulsion of GI contents resulting from Secretory, osmotic, motor and exudative diar-
contractions of gut and thoracoabdominal wall rhoea may be distinguished [61], but in the ICU
musculature [46]. Vomiting is contrasted with it is often better to distinguish between disease-,
regurgitation, which is the effortless passage of food/feeding- and drug-related diarrhoea [61,
gastric contents into the mouth [46]. In ICU 62].
patients the forcefulness of the act is often not Management Symptomatic therapyreplace-
detectable; therefore, regurgitation and vomiting ment of fluids and electrolytes, haemodynamic
should be assessed together. stabilization and organ protection (e.g. correction
Management Several guidelines for prevention of hypovolaemia to prevent impairment of renal
and management of postoperative nausea and function) forms the basic management [61, 63,
vomiting are available [4751]. However, no 64] (grade 1D). At the same time, trigger
studies have addressed management of vomiting mechanisms need to be discovered and when
in mechanically ventilated ICU patients; there- possible stopped (e.g. laxatives, sorbitol, lactu-
fore, no specific recommendation can be given. lose, antibiotics) or treated (e.g. malabsorption,
5.2 Gastric residual volume could be considered high if inflammatory bowel disease). Feeding-related
a single volume exceeds 200 ml [5254]. diarrhoea in critically ill patients may require
Rationale There is no sufficient scientific evi- reduction of infusion rate, repositioning of
dence or physiological ground to define precise feeding tube, or dilution of nutrition formula.
values for high gastric residuals [53, 55]. Mea- Changing formula by adding soluble fibre pro-
surement of gastric residuals is neither longs transit time [61, 6466] (grade1C). Only in
standardized nor validated [56]. It has been cases of severe or recurrent Clostridium difficile-
suggested that gastric residual volume greater associated diarrhoea is oral vancomycin superior
than 200 ml should prompt careful bedside to metronidazole [6769] (grade 2C).
evaluation, but automatic cessation of enteral 5.4 GI bleeding is any bleeding into the GI tract lumen,
nutrition solely on the basis on residual volumes confirmed by macroscopic presence of blood in
of 200500 ml should be avoided [53, 56, 57]. vomited fluids, gastric aspirate or stool.
Despite the lack of scientific evidence, the Rationale Asymptomatic, endoscopically evident
members of the WGAP arbitrarily use total mucosal damage occurs in the majority of ICU
volumes of gastric residuals above 1,000 ml/ patients [2]. Clinically evident GI bleeding
24 h as a sign of abnormal gastric emptying, reflecting considerable damage to GI mucosa
which requires specific attention. may be seen in 525% of ICU patients [2].
Management Intravenous administration of met- Clinically important bleeding, defined as overt
oclopramide and/or erythromycin is bleeding in association with haemodynamic
recommended for management of high gastric compromise or the need for blood transfusions
residuals, whereas cisapride is no longer [70], occurs in 1.54% of mechanically venti-
approved [58] (grade 1B). Routine use of lated patients [2, 70, 71].
motility agents is not recommended [58] (grade Management In cases of clinically evident GI
1A). Acupuncture stimulation may facilitate bleeding, the haemodynamic status dictates the
gastric empting in neurosurgical ICU patients approach. In cases of bleeding with haemody-
[59] (grade 2B). Use of opioids and deep namic instability endoscopy is the diagnostic tool
sedation should be avoided/reduced if possible. of choice [72], but when bleeding is ongoing and
Cessation of gastric feeding is suggested if massive, precluding adequate endoscopic assess-
residual volumes exceed 500 ml per single ment, angiography is appropriate (grade 2C).
measurement [57]. Here, postpyloric feeding Early upper GI endoscopy (less than 24 h) is
should be considered [58] (grade 2D). Routine recommended [72, 73] (grade 1A), except for
application of postpyloric feeding is not advo- patients with acute variceal bleeding in whom a
cated [58] (grade 2D). Postpyloric feeding may more expedite procedure (less than 12 h) should
cause severe small bowel dilatation and perfora- be considered [74] (grade 2C). Epinephrine
tion in rare cases. injection can be used in combination with
389

another method, such as clips, thermocoagula- quadrants, repeated at least once within a tight
tion or sclerosant injection [72] (grade 1A). time frame. Palpation of the abdomen before the
Routine second endoscopy is not recommended, auscultation may stimulate peristalsis causing
but in cases of rebleeding, a second attempt for subsequent bowel sounds that may not have been
endoscopic therapy is recommended [72] (grade there otherwise [82].
1A). In cases of a negative upper endoscopy with
evidence of GI bleeding, colonoscopy should be 5.6.1 Absent peristalsisno bowel sounds are heard at
performed, followed by small bowel exploration cautious auscultation.
using push enteroscopy if colonoscopy is nega- Rationale Complete lack of bowel
tive [75] (grade 2C). In cases of ongoing sounds is abnormal [83]. However, it
bleeding with negative endoscopies, abdominal should be recognized that presence of
surgery with intraoperative endoscopy or inter- bowel sounds does not confirm normal
ventional radiology should be considered [76, motility, and that reoccurrence of bowel
77] (grade 2C). sounds does not correlate with improve-
5.5 Paralysis of lower GI tract (paralytic ileus) is the ment of paralysis.
inability of the bowel to pass stool due to 5.6.2 Hyperperistalsis is present if excessive bowel
impaired peristalsis. Clinical signs include sounds are heard on auscultation.
absence of stool for three or more consecutive Rationale Hyperperistalsis is a state of
days without mechanical obstruction. Bowel excessive motility of the digestive tract.
sounds may or may not be present. It can be present during bowel obstruc-
Rationale Outside of the ICU, the terms consti- tion occurring in parts of the bowel as
pation and obstipation include uncomfortable or attempts to overcome obstruction [84].
infrequent bowel movements, hard stool and Management There are no special man-
painful defecation. Because these symptoms may agement suggestions for absent/abnormal
not be expressed in ICU patients, it is suggested bowel sounds.
to use the term paralysis of lower GI tract. A cut- 5.7 Bowel dilatation is present if colonic diameter
off level of 3 days has been used in most of the exceeds 6 cm (greater than 9 cm for caecum) or
epidemiological ICU studies [78, 79]. small bowel diameter exceeds 3 cm, diagnosed
Management Inhibitory drugs for GI motility either on plain abdominal X-ray or CT scan [85,
(e.g. catecholamines, sedatives, opioids) must be 86].
withdrawn if possible and conditions impairing Rationale Bowel dilatation is a common sign in
motility (e.g. hyperglycemia, hypokalaemia) obstruction at any level of the GI tract. Bowel
corrected [1921] (grade 1C). Because of their dilatation may also appear without an obstruc-
delayed onset of action, laxative drugs must be tion; the terms toxic megacolon following colitis
started early or given prophylactically [24, 25] and acute colonic pseudo-obstruction or Ogil-
(grade 1D). vies syndrome, are used to describe acute severe
Because of unknown long-term efficacy and colonic dilatation.
safety the routine use of opioid antagonists Management Next to the correction of fluid and
cannot be recommended [80, 81] (grade 2B). electrolyte imbalance, nasogastric decompres-
Prokinetics like domperidone, metoclopramide sion may be helpful [29, 87] (grade 1D),
and erythromycin are used to stimulate the upper although routine usage of nasogastric tubes after
GI tract (stomach and small bowel), whereas elective laparotomy is not recommended [88]
neostigmine stimulates small bowel and colonic (grade 1A). After exclusion of mechanical
motility [25, 30]. Despite the lack of well- obstruction, intravenous neostigmine could be
controlled studies and sufficient evidence, we considered in patients with a caecal diameter
recommend a standardised approach in using [10 cm and without improvement within 24 h
prokinetics for management of motility disorders [29, 89] (grade 2B). Colonoscopy is recom-
[24, 25] (grade 1D). mended for non-surgical decompression in
5.6 Abnormal bowel sounds patients with a caecal diameter [10 cm and no
Rationale Normal frequency of bowel sounds improvement after 2448 h of conservative
may range between 5 and 35 sounds/min [82]; treatment [29, 87, 90] (grade 1C). Colonoscopic
the clinical significance of abnormal bowel decompression is effective in up to 80%, but
sounds is not clear. No technique of auscultation carries a certain morbidity/mortality risk [30].
has been proven to be superior [83]. The authors Conservative treatment together with colonos-
suggest auscultation for at least 1 min in two copy may be continued for 4872 h unless the
390

caecum is [12 cm wide [30, 91] (grade 2C). [95]. European Society for Parenteral and Enteral
In cases of unresponsiveness to conservative Nutrition (ESPEN) guidelines are available with
treatment, surgery is indicated due to the threat- recommendations for nutrition in intensive care [58].
ening risk of perforation [29, 30] (grade 1D). Feeding protocols based on these guidelines should be
Usage of a laparoscopic technique with thoracic implemented in every institution. Periods of interrup-
epidural anaesthesia where appropriate enhances tion of enteral feeding due to various interventions in
bowel function after abdominal surgery [9294] the hospital (surgery, diagnostic or therapeutic inter-
(grade 1B), and may therefore prevent bowel ventions, extubation) should be remembered and
dilatation. minimized [96, 97]. Daily assessment of adequacy of
6. Feeding protocols enteral nutrition is required.
Decreased food intake and resulting malnutrition 7. A schematic guideline for the management of patients
are independent risk factors for in-hospital mortality with AGI is presented in Fig. 1.

Fig. 1 Schematic guideline for Guideline for diagnosis and management of AGI
the management of patients
with AGI. EF enteral feeding, Enteral feeding >80% of calculated needs Aim 100 % of calculated needs
yes
EN enteral nutrition, PN Check prescribed vs. delivered
parenteral nutrition Re-evaluate daily
no

Re-evaluate at least daily


Shock? yes
Start minimal EF (20 ml/h)

no

Re-evaluate at least daily


EF contraindicated? yes Consider parenteral feeding

no
Severe, general condition not
improving
GI symptoms present? yes

AGI I Moderate, expectedly self-limited


no Start/increase EF
Use protocol
Re-evaluate daily AGI II
Increase EF
Start therapy according to the
Re-evaluate daily
symptom (e.g. prokinetics)
Measure IAP
Start minimal enteral feeding
Feeding intolerance? yes Consider postpyloric feeding

no  Increase EF
yes Condition improving? no
 Re-evaluate

No AGI AGI III


Aim 100 % of calculated needs Search for undiagnosed abdominal
Check prescribed vs. delivered pathology
Re-evaluate daily Continue therapy according to the
symptom (e.g. prokinetics)
Treat IAH
Try (challenge) minimal EF and start PN
Critical decompensation through AGI?

AGI IV
yes
Intervention
391

Discussion we need to move forward, and we suggest to start with the


definitions proposed in this paper.
Terminology and definitions provided in the present paper
were developed with the aim of providing clinical definitions
which may be used in different ICUs and clinical situations.
Our working methods were similar to those commonly Summary
used for the consensus definitions and grading of evidence
for the treatment recommendations. The main limitation The terminology and definitions provided herein should
of the current document is the lack of objective measures allow better clinical communication as well as compar-
for GI function/dysfunction. As the evidence in this field ison between future studies. Defining the specific
is scarce, the definitions are largely based on expert variables is the first step in a process towards better
opinion. Therefore, in case new established measures to knowledge in this area. We propose a definition of acute
assess GI function/dysfunction become available, pro- gastrointestinal injury (AGI) with four grades of sever-
posed definitions need to be revised. The complete ity. AGI grade I stands for a self-limiting condition with
description of diagnostic procedures for conditions increased risk of developing GI dysfunction or failure;
underlying AGI is not provided in the current manuscript, AGI grade II (GI dysfunction) is a condition requiring
common clinical approach is presumed. interventions to restore GI function; AGI grade III (GI
Our grading system is not based on a certain numeric failure) is a condition when GI function cannot be
variable and is not validated. With no doubt further restored with interventions; and AGI grade IV is dra-
research is needed to establish the measures of GI function matically manifesting GI failure, which is immediately
that could be used in a reproducible manner for grading GI life-threatening.
function. At present, the descriptions of the grades of AGI The WGAP of ESICM suggests using the proposed
are complicated and the same grade of AGI may have definitions until the results of a broader consensus are
different clinical expressions. It is likely that the score will available. We encourage research to define explicit
in some extent be dependent on the treatment applied. In characteristics of GI function in critically ill patients.
fact, other organ dysfunction scores (e.g. SOFA score)
have also been developed first, and only validated after- Acknowledgment We thank Luigi Camporota for his contribution.
wards. Moreover, the cardiovascular sub-score of SOFA
Conflicts of interest None.
[13], known to be the most performing among all the sub-
scores, is defined as a mean arterial pressure and the usage/ Open Access This article is distributed under the terms of the Cre-
dosage of vasoactive/inotropic agents, where the last part ative Commons Attribution License which permits any use,
is clearly dependent on the local treatment traditions. distribution, and reproduction in any medium, provided the original
Despite the many well-known limitations which have author(s) and the source are credited.
been restraining the development in this area for so long,

References
1. Rombeau JL, Takala J (1997) Summary 5. Reintam A, Parm P, Kitus R, Starkopf J, 8. Piton G, Manzon C, Cypriani B,
of round table conference: gut Kern H (2008) Gastrointestinal failure Carbonnel F, Capellier G (2011) Acute
dysfunction in critical illness. Intensive score in critically ill patients: a intestinal failure in critically ill patients:
Care Med 23:476479 prospective observational study. Crit is plasma citrulline the right marker?
2. Mutlu GM, Mutlu EA, Factor P (2001) Care 12:R90 Intensive Care Med 37:911917
GI complications in patients receiving 6. Nguyen NQ, Lam SW, Ching K, 9. Kumar A, Roberts D, Wood KE, Light
mechanical ventilation. Chest Chapman M, Fraser RJ, Holloway RH B, Parrillo JE, Sharma S, Suppes R,
119:12221241 (2007) Gastric feed intolerance is not Feinstein D, Zanotti S, Taiberg L,
3. Reintam A, Parm P, Kitus R, Kern H, increased in critically ill patients with Gurka D, Kumar A, Cheang M (2006)
Starkopf J (2009) Gastrointestinal type II diabetes mellitus. Intensive Care Duration of hypotension before
symptoms in intensive care patients. Med 33:17401745 initiation of effective antimicrobial
Acta Anaesthesiol Scand 53:318324 7. Lebuffe G, Vallet B, Takala J, Hartstein therapy is the critical determinant of
4. Montejo JC (1999) Enteral nutrition- G, Lamy M, Mythen M, Bakker J, survival in human septic shock. Crit
related gastrointestinal complications in Bennet D, Boyd O, Webb A (2004) A Care Med 34:15891596
critically ill patients: a multicenter European multicenter, observational 10. Jones AE, Brown MD, Trzeciak S,
study. The Nutritional and Metabolic study to assess the value of gastric-to- Shapiro NI, Garrett JS, Heffner AC,
Working Group of the Spanish Society end tidal PCO2 difference in predicting Kline JA (2008) The effect of a
of Intensive Care Medicine and postoperative complications. Anesth quantitative resuscitation strategy on
Coronary Units. Crit Care Med Analg 99:166172 mortality in patients with sepsis: a meta-
27:14471453 analysis. Crit Care Med 36:27342739
392

11. Dellinger RP, Levy MM, Carlet JM, 18. Antonelli M, Azoulay E, Bonten M, 27. Casaer MP, Mesotten D, Hermans G,
Bion J, Parker MM, Jaeschke R, Chastre J, Citerio G, Conti G, De Wouters PJ, Schetz M, Meyfroidt G,
Reinhart K, Angus DC, Brun-Buisson Backer D, Lemaire F, Gerlach H, Van Cromphaut S, Ingels C,
C, Beale R, Calandra T, Dhainaut JF, Hedenstierna G, Joannidis M, Macrae Meersseman P, Muller J, Vlasselaers D,
Gerlach H, Harvey M, Marini JJ, D, Mancebo J, Maggiore SM, Mebazaa Debaveye Y, Desmet L, Dubois J, Van
Marshall J, Ranieri M, Ramsay G, A, Preiser JC, Pugin J, Wernerman J, Assche A, Vanderheyden S, Wilmer A,
Sevransky J, Thompson BT, Townsend Zhang H (2009) Year in review in Van den Berghe G (2011) Early versus
S, Vender JS, Zimmerman JL, Vincent intensive care medicine 2009: I. late parenteral nutrition in critically ill
JL, International Surviving Sepsis Pneumonia and infections, sepsis, adults. N Engl J Med 365(6):506517
Campaign Guidelines Committee outcome, acute renal failure and acid 28. Balogh Z, Moore FA, Goettler CE,
(2008) Surviving sepsis campaign: base, nutrition and glycaemic control. Rotondo MF, Schwab CW, Kaplan MJ
international guidelines for Intensive Care Med 36(2):196209 (2006) Management of abdominal
management of severe sepsis and septic 19. Fruhwald S, Scheidl S, Toller W, compartment syndrome. In: Ivatury R,
shock: 2008. Crit Care Med 36:296327 Petnehazy T, Holzer P, Metzler H, Cheatham M, Malbrain M, Sugrue M
12. ARDS Network (2000) Ventilation with Hammer HF (2000) Low potential of (eds) Abdominal compartment
lower tidal volumes as compared with dobutamine and dopexamine to block syndrome. Landes Bioscience,
traditional tidal volumes for acute lung intestinal peristalsis as compared with Georgetown, pp 264294
injury and the acute respiratory distress other catecholamines. Crit Care Med 29. Saunders MD, Kimmey MB (2005)
syndrome. N Engl J Med 28(8):28932897 Systematic review: acute colonic
342:13011308 20. Nguyen NQ, Chapman MJ, Fraser RJ, pseudo-obstruction. Aliment Pharmacol
13. Vincent JL, Moreno R, Takala J, Bryant LK, Burgstad C, Ching K, Ther 22:917925
Willatts S, De Mendonca A, Bruining Bellon M, Holloway RH (2008) The 30. De Giorgio R, Barbara G, Stanghellini
H, Reinhart CK, Suter PM, Thijs LG effects of sedation on gastric emptying V, Tonini M, Vasina V, Cola B,
(1996) The SOFA (sepsis-related organ and intra-gastric meal distribution in Corinaldesi R, Biagi G, De Ponti F
failure assessment) score to describe critical illness. Intensive Care Med (2001) Review article: the
organ dysfunction/failure. On behalf of 34(3):454460 pharmacological treatment of acute
the Working Group on Sepsis-Related 21. Fruhwald S, Herk E, Petnehazy T, colonic pseudo-obstruction. Aliment
Problems of the European Society of Scheidl S, Holzer P, Hammer F, Pharmacol Ther 15:17171727
Intensive Care Medicine. Intensive Metzler H (2002) Sufentanil potentiates 31. Heyland D, Cook DJ, Winder B,
Care Med 22:707710 the inhibitory effect of epinephrine on Brylowski L, Van deMark H, Guyatt G
14. Bone RC, Balk RA, Cerra FB, intestinal motility. Intensive Care Med (1995) Enteral nutrition in the critically
Dellinger RP, Fein AM, Knaus WA, 28:7480 ill patient: a prospective survey. Crit
Schein RM, Sibbald WJ (1992) 22. McArthur CJ, Gin T, McLaren IM, Care Med 23:10551060
Definitions for sepsis and organ failure Critchley JA, Oh TE (1995) Gastric 32. MacLaren R, Kuhl DA, Gervasio JM,
and guidelines for the use of innovative emptying following brain injury: effects Brown RO, Dickerson RN, Livingston
therapies in sepsis. The ACCP/SCCM of choice of sedation and intracranial TN, Swift K, Headley S, Kudsk KA,
Consensus Conference Committee. pressure. Intensive Care Med Lima JJ (2000) Sequential single doses
American College of Chest Physicians/ 21(7):573576 of cisapride, erythromycin, and
Society of Critical Care Medicine. 23. Cheatham ML, Malbrain ML, metoclopramide in critically ill patients
Chest 101:16441655 Kirkpatrick A, Sugrue M, Parr M, De intolerant to enteral nutrition: a
15. Schunemann HJ, Jaeschke R, Cook DJ, Waele J, Balogh Z, Leppaniemi A, randomized, placebo-controlled,
Bria WF, El-Solh AA, Ernst A, Fahy Olvera C, Ivatury R, DAmours S, crossover study. Crit Care Med
BF, Gould MK, Horan KL, Krishnan Wendon J, Hillman K, Wilmer A 28:438444
JA, Manthous CA, Maurer JR, (2007) Results from the international 33. MacLaren R, Patrick WD, Hall RI,
McNicholas WT, Oxman AD, conference of experts on intra- Rocker GM, Whelan GJ, Lima JJ
Rubenfeld G, Turino GM, Guyatt G, abdominal hypertension and abdominal (2001) Comparison of cisapride and
ATS Documents Development compartment syndrome. II. metoclopramide for facilitating gastric
Implementation Committee (2006) An Recommendations. Intensive Care Med emptying and improving tolerance to
official ATS statement: grading the 33:951962 intragastric enteral nutrition in critically
quality of evidence and strength of 24. Fruhwald S, Holzer P, Metzler H (2008) III, mechanically ventilated adults. Clin
recommendations in ATS guidelines Gastrointestinal motility in acute Ther 23:18551866
and recommendations. Am J Respir Crit illness. Wien Klin Wochenschr 34. Mentec H, Dupont H, Bocchetti M,
Care Med 174:605614 120:617 Cani P, Ponche F, Bleichner G (2001)
16. Fruhwald S, Kainz J (2010) Effect of 25. Herbert MK, Holzer P (2008) Upper digestive intolerance during
ICU interventions on gastrointestinal Standardized concept for the treatment enteral nutrition in critically ill patients:
motility. Curr Opin Crit Care of gastrointestinal dysmotility in frequency, risk factors, and
16:159164 critically ill patientscurrent status and complications. Crit Care Med
17. Doig GS, Heighes PT, Simpson F, future concepts. Clin Nutr 27:2541 29:19551961
Sweetman EA, Davies AR (2009) Early 26. Nguyen NQ, Chapman M, Fraser RJ, 35. Thibault R, Pichard C (2010) Parenteral
enteral nutrition, provided within 24 h Bryant LK, Burgstad C, Holloway RH nutrition in critical illness: can it safely
of injury or intensive care unit (2007) Prokinetic therapy for feed improve outcomes? Crit Care Clin
admission, significantly reduces intolerance in critical illness: 1 drug or 26:467480
mortality in critically ill patients: a two? Crit Care Med 35:25612567 36. Wernerman J (2008) Paradigm of early
meta-analysis of randomised controlled parenteral nutrition support in
trials. Intensive Care Med combination with insufficient enteral
35:20182027 nutrition. Curr Opin Clin Nutr Metab
Care 11:160163
393

37. Malbrain ML, Cheatham ML, 47. Apfel CC, Kranke P, Piper S, Rusch D, 56. McClave SA, Snider HL (2002)
Kirkpatrick A, Sugrue M, Parr M, De Kerger H, Steinfath M, Stocklein K, Clinical use of gastric residual volumes
Waele J, Balogh Z, Leppaniemi A, Spahn DR, Mollhoff T, Danner K, as a monitor for patients on enteral tube
Olvera C, Ivatury R, DAmours S, Biedler A, Hohenhaus M, Zwissler B, feeding. J Parenter Enteral Nutr
Wendon J, Hillman K, Johansson K, Danzeisen O, Gerber H, Kretz FJ 26:4348
Kolkman K, Wilmer A (2006) Results (2007) Nausea and vomiting in the 57. Montejo JC, Minambres E, Bordeje L,
from the international conference of postoperative phase. Expert- and Mesejo A, Acosta J, Heras A, Ferre M,
experts on intra-abdominal evidence-based recommendations for Fernandez-Ortega F, Vaquerizo CI,
hypertension and abdominal prophylaxis and therapy. Anaesthesist Manzanedo R (2010) Gastric residual
compartment syndrome. I. Definitions. 56:11701180 volume during enteral nutrition in ICU
Intensive Care Med 32:17221732 48. Gomez-Arnau JI, Aguilar JL, Bovaira patients: the REGANE study. Intensive
38. De Keulenaer BL, De Waele JJ, Powell P, Bustos F, De Andres J, de la Pinta Care Med 36(8):13861396
B, Malbrain ML (2009) What is normal JC, Garca-Fernandez J, Lopez-Alvarez 58. Kreymann KG, Berger MM, Deutz NE,
intra-abdominal pressure and how is it S, Lopez-Olaondo L, Neira F, Planas A, Hiesmayr M, Jolliet P, Kazandjiev G,
affected by positioning, body mass and Pueyo J, Vila P, Torres LM (2010) Nitenberg G, van den Berghe G,
positive end-expiratory pressure? Postoperative nausea and vomiting and Wernerman J, Ebner C, Hartl W,
Intensive Care Med 35:969976 opioid-induced nausea and vomiting: Heymann C, Spies C (2006) ESPEN
39. Malbrain ML, De laet I, Cheatham M guidelines for prevention and treatment. guidelines on enteral nutrition:
(2007) Consensus conference Rev Esp Anestesiol Reanim intensive care. Clin Nutr 25:210223
definitions and recommendations on 57:508524 59. Pfab F, Winhard M, Nowak-Machen M,
intra-abdominal hypertension (IAH) 49. Diemunsch P (2008) Conference of Napadow V, Irnich D, Pawlik M, Bein
and the abdominal compartment expertsshort text. Management of T, Hansen E (2011) Acupuncture in
syndrome (ACS)the long road to the postoperative nausea and vomiting. critically ill patients improves delayed
final publications, how did we get French society of anesthesia and gastric emptying: a randomized
there? Acta Clin Belg Suppl 62:4459 resuscitation. Ann Fr Anesth Reanim controlled trial. Anesth Analg
40. Hakobyan RV, Mkhoyan GG (2008) 27:866878 112:150155
Epidural analgesia decreases 50. McCracken G, Houston P, Lefebvre G 60. Lankisch PR, Mahlke R, Lubbers H,
intraabdominal pressure in (2008) Guideline for the management Lembcke B, Rosch W (2006)
postoperative patients with primary of postoperative nausea and vomiting. Zertifizierte medizinische fortbildung:
intra-abdominal hypertension. Acta J Obstet Gynaecol Can leitsymptom diarrho. Deutsches
Clin Belg 63:8692 30(6007):608616 Arzteblatt 103:261269
41. De Laet I, Hoste E, Verholen E, De 51. Gan TJ, Meyer TA, Apfel CC, Chung F, 61. Wiesen P, Van Gossum A, Preiser JC
Waele JJ (2007) The effect of Davis PJ, Habib AS, Hooper VD, (2006) Diarrhoea in the critically ill.
neuromuscular blockers in patients with Kovac AL, Kranke P, Myles P, Philip Curr Opin Crit Care 12:149154
intra-abdominal hypertension. Intensive BK, Samsa G, Sessler DI, Temo J, 62. Sabol VK (2007) Diarrhea, applying
Care Med 33:18111814 Tramer MR, Vander Kolk C, Watcha M research to bedside practice. AACN
42. De Waele JJ, Hoste EA, Malbrain ML (2007) Society for ambulatory Adv Crit Care 1:3244
(2006) Decompressive laparotomy for anesthesia guidelines for the 63. Pawlowsky SW, Warren CA, Guerrant
abdominal compartment syndromea management of postoperative nausea R (2009) Diagnosis and treatment of
critical analysis. Crit Care. 10:R51 and vomiting. Anesth Analg acute or persistent diarrhea.
43. De Waele J, Desender L, De laet I, 105:16151628 Gastroenterology 136:18741886
Ceelen W, Pattyn P, Hoste E (2010) 52. White H, Sosnowski K, Tran K, Reeves 64. Whelan K, Schneider SM (2011)
Abdominal decompression for A, Jones M (2009) A randomised Mechanisms, prevention, and
abdominal compartment syndrome in controlled comparison of early post- management of diarrhea in enteral
critically ill patients: a retrospective pyloric versus early gastric feeding to nutrition. Curr Opin Gastroenterol
study. Acta Clin Belg 656:396400 meet nutritional targets in ventilated 27:152159
44. Rasmussen TE, Hallett JW, Noel AA, intensive care patients. Crit Care 65. Rushdi TA, Pichard C, Khater YH
Jenkins G, Bower C, Cherry KJ, 13:R187 (2004) Control of diarrhoea by fibre-
Panneton JM, Gloviczki P (2002) Early 53. McClave SA, Martindale RG, Vanek enriched diet in ICU patients on enteral
abdominal closure with mesh reduces VW, McCarthy M, Roberts P, Taylor B, nutrition: a prospective randomized
multiple organ failure after ruptured Ochoa JB, Napolitano L, Cresci G, The controlled trial. Clin Nutr
abdominal aortic aneurysm repair: A.S.P.E.N. Board of Directors and the 23:13441352
guidelines from a 10-year casecontrol American College of Critical Care 66. Nakao M, Ogura Y, Satake S, Ito I,
study. J Vasc Surg 35:246253 Medicine (2009) Guidelines for the Iguchi A, Takagi K, Nabeshima T
45. Mayberry JC, Mullins RJ, Crass RA, provision and assessment of nutrition (2002) Usefulness of soluble dietary
Trunkey DD (1997) Prevention of support therapy in the adult critically ill fibre for the treatment of diarrhoea
abdominal compartment syndrome by patient. J Parenter Enteral Nutr during enteral nutrition in elderly
absorbable mesh prosthesis closure. 33:277316 patients. Nutrition 18:3539
Arch Surg. 132:957961 54. Neumann DA, DeLegge MH (2002) 67. Zar FA, Bakkanagari SR, Moorthi KM,
46. Fauci AS, Braunwald E, Kasper DL, Gastric versus small-bowel tube feeding Davis MB (2007) A comparison of
Hauser SL, Longo DL, Jameson JL, in the intensive care unit: a prospective vancomycin and metronidazole for the
Loscalzo J (eds) (2007) Harrisons comparison of efficacy. Crit Care Med treatment of Clostridium difficile-
principles of internal medicine, 17th 30:14361438 associated diarrhea, stratified by disease
edn. McGraw-Hill, USA 55. Hurt RT, McClave SA (2010) Gastric severity. Clin Infect Dis 45:302307
residual volumes in critical illness: what 68. Leffler DA, Lamont JT (2009)
do they really mean? Crit Care Clin Treatment of Clostridium difficile-
26:481490 associated disease. Gastroenterology
136:18991912
394

69. Aslam S, Hamill RJ, Musher DM 77. Ripoll C, Banares R, Beceiro I, 88. Cheatham ML, Chapman WC, Key SP,
(2005) Treatment of Clostridium Menchen P, Catalina MV, Echenagusia Sawyers JL (1995) A meta-analysis of
difficile-associated disease: old A, Turegano F (2004) Comparison of selective versus routine nasogastric
therapies and new strategies. Lancet transcatheter arterial embolization and decompressiom after elective
Infect Dis 5:549557 surgery for treatment of bleeding peptic laparotomy. Ann Surg 221:469478
70. Cook DJ, Fuller HD, Gyatt GH, ulcer after endoscopic treatment failure. 89. Ponec RJ, Saunders MD, Kimmey MB
Marshall JC, Leasa D, Hall R, Winton Vasc Interv Radiol 15:447450 (1999) Neostigmine for the treatment of
TL, Rutledge F, Todd TJ, Roy P et al 78. Nassar AP Jr, da Silva FM, de Cleva R acute colonic pseudo-obstruction.
(1994) Risk factors for gastrointestinal (2009) Constipation in intensive care N Engl J Med 341:137141
bleeding in critically ill patients. unit: incidence and risk factors. J Crit 90. Jetmore AB, Timmcke AE, Gathright
Canadian Critical Care Trials Group. Care 24:630.e9630.e12 JB Jr, Hicks TC, Ray JE, Baker JW
N Engl J Med 330:377381 79. Mostafa SM, Bhandari S, Ritchie G, (1992) Ogilvies syndrome:
71. Mayr VD, Duenser MW, Greil V, Gratton N, Wenstone R (2003) colonoscopic decompression and
Jochberger S, Luckner G, Ulmer H, Constipation and its implications in the analysis of predisposing factors. Dis
Friesenecker BE, Takala J, Hasibeder critically ill patient. Br J Anaesth Colon Rectum 35:11351142
WR (2006) Causes and determinants of 91:815819 91. Dorudi S, Berry AR, Kettlewell MG
outcome in critically ill patients. Crit 80. McNicol E, Boyce DB, Schumann R, (1992) Acute colonic pseudo-
Care 10:R14 Carr D (2008) Mu-opioid antagonists obstruction. Br J Surg 79:99103
72. Barkun AN, Bardou M, Kuipers EJ, for opioid induced bowel dysfunction. 92. Johnson MD, Walsh RM (2009)
Sung J, Hunt RH, Martel M, Sinclair P, Cochrane Database Syst Rev Current therapies to shorten
International Consensus Upper CD006332 postoperative ileus. Cleveland Clin J
Gastrointestinal Bleeding Conference 81. Holzer P (2010) Opioid antagonists for Med 76:641648
Group (2010) International consensus prevention and treatment of opioid- 93. Jrgensen H, Wetterslev J, Miniche S,
recommendations on the management induced gastrointestinal effects. Curr Dahl JB (2000) Epidural local
of patients with nonvariceal upper Opin Anaesthesiol 23:616622 anaesthetics versus opioid-based
gastrointestinal bleeding. Ann Intern 82. Bickley LS, Syilagyi PG (2009) Bates analgesic regimens on postoperative
Med 152:101113 guide to physical examination and gastrointestinal paralysis, PONV and
73. Cooper GS, Chak A, Way LE, Hammar history taking, 10th edn. Lippincott pain after abdominal surgery. Cochrane
PJ, Harper DL, Rosenthal GE (1999) Williams & Wilkins, Philadelphia Database Syst Rev 4:CD001893
Early endoscopy in upper 83. Baid H (2009) A critical review of 94. Freise H, Fischer LG (2009) Intestinal
gastrointestinal hemorrhage: auscultating bowel sounds. Br J Nurs effects of thoracic epidural anesthesia.
associations with recurrent bleeding, 18:18 Curr Opin Anaesthesiol 22:644648
surgery, and length of hospital stay. 84. Kahan S, Miller R, Smith EG (2009) In 95. Hiesmayr M, Schindler K, Pernicka E,
Gastrointest Endosc 49:145152 a page: signs and symptoms, 2nd edn. Schuh C, Schoeninger-Hekle A, Bauer
74. de Franchis R, Baveno V Faculty Lippincott Williams & Wilkins, P, Laviano A, Lovell AD, Mouhieddine
(2010) Revising consensus in portal Philadelphia M, Schuetz T, Schneider SM, Singer P,
hypertension: report of the Baveno V 85. Sheth SG, LaMont JT (1998) Toxic Pichard C, Howard P, Jonkers C, Grecu
consensus workshop on methodology of megacolon. Lancet 351:509513 I, Lingqvist O, The Nutrition Day Team
diagnosis and therapy in portal 86. Krajewski K, Siewert B, Eisenberg RL (2009) Decreased food intake is a risk
hypertension. J Hepatology 53:762768 (2009) Colonic dilation. AJR Am J factor for mortality in hospitalised
75. Sidhu R, Sanders DS, Morris AJ, Roentgenol 193:363372 patients: the nutrition day survey 2006.
McAlindon ME (2008) Guidelines on 87. Eisen GM, Baron TH, Dominitiz JA, Clin Nutr 28:484491
small bowel enteroscopy and capsule Faigel DO, Goldstein JL, Johanson JF, 96. Rice TW, Swope T, Bozeman S,
endoscopy in adults. Gut 57:125136 Mallery JS, Raddawi HM, Vargo JJ, Wheeler AP (2005) Variation in enteral
76. Eriksson LG, Ljungdahl M, Sundbom Waring JP, Fanelli RD, Wheeler- nutrition delivery in mechanically
M, Nyman R (2008) Transcatheter Harbaugh J, Standards of Practice ventilated patients. Nutrition
arterial embolisation versus surgery in Committee of the American Society for 21:786792
the treatment of upper gastrointestinal Gastrointestinal Endoscopy (2002) 97. Schneider JA, Lee YJ, Grubb WR,
bleeding after therapeutic endoscopy Acute colonic pseudo-obstruction. Denny J, Hunter C (2009) Institutional
failure. J Vasc Interv Radiol Gastrointest Endosc 56:789792 practices of withholding enteral feeding
19:14131418 from intubated patients. Crit Care Med
37:22992302