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Clinical Nutrition
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Review
a r t i c l e i n f o
s u m m a r y
Article history:
Received 25 July 2014
Accepted 5 November 2014
Background & aims: Enteral nutrition is important in critically ill patients and is usually administered via
a nasogastric tube. As gastric emptying is frequently delayed, and this compromises the delivery of
nutrient, it is important that the emptying rate can be quantied.
Methods: A comprehensive search of MEDLINE/PubMed, of English articles, from inception to 1 July 2014.
References of included manuscripts were also examined for additional studies.
Results: A number of methods are available to measure gastric emptying and these broadly can be
categorised as direct- or indirect-test and surrogate assessments. Direct tests necessitate visualisation of
the stomach contents during emptying and are unaffected by liver or kidney metabolism. The most
frequently used direct modality is scintigraphy, which remains the gold standard. Indirect tests use a
marker that is absorbed in the proximal small intestine, so that measurements of the marker, or its
metabolite measured in plasma or breath, correlates with gastric emptying. These tests include drug and
carbohydrate absorption and isotope breath tests. Gastric residual volumes (GRVs) are used frequently to
quantify gastric emptying during nasogastric feeding, but these measurements may be inaccurate and
should be regarded as a surrogate measurement. While the inherent limitations of GRVs make them less
suitable for research purposes they are often the only technique that is available for clinicians at the
bedside.
Conclusions: Each of the available techniques has its strength and limitations. Accordingly, the choice of
gastric emptying test is dictated by the particular requirement(s) and expertise of the investigator or
clinician.
2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
Keywords:
Gastric emptying
Intensive care
Critically ill
Enteral nutrition
1. Introduction
Enteral nutrition is part of standard care for critically ill patients
and is most commonly delivered via the gastric route [1].
Frequently, however, nutritional targets are not achieved via the
gastric route, particularly because of critical illness induced
gastrointestinal dysmotility, which leads to slow gastric emptying
[2]. While the prevalence and magnitude of delayed gastric
emptying in the critically ill are inconsistently reported [3e5],
possibly because these variables are dependent on the precision of
the methodology used to measure gastric emptying, as well as the
* Corresponding author. Intensive Care Unit, Level 4, Royal Adelaide Hospital,
North Terrace, Adelaide 5000, South Australia, Australia. Tel.: 61 8 8222 4624, 61
401 878 997.
E-mail address: p_kar@hotmail.com (P. Kar).
http://dx.doi.org/10.1016/j.clnu.2014.11.003
0261-5614/ 2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
558
Table 1
Methods of gastric emptying measurement in the critically ill.
Type
Method
Direct
Indirect
Scintigraphy
Drug absorption
Carbohydrate absorption (3-O-Methylglucose; 3-OMG)
Isotope breath test
Ultrasound
MRI
Gastric residual volumes (GRVs)
Other
Surrogate
2.3. Scintigraphy
Scintigraphy is regarded as the gold standard technique to
measure gastric emptying [19]. A substrate labelled with a radioactive marker is placed in the stomach. This meal can be solid or
liquid, and the liquid can be nutrient or non-nutrient. In the critically ill, liquid nutrient is the constituent of most interest. The
disappearance of the radiolabelled meal component from the eld
of view is measured over time with either a xed or mobile gamma
camera, tted with a large eld-of-view collimator.
The choice of radioisotope is crucial to the success of the measurements. It should be non-toxic, impermeable to the gastric
mucosa, and homogenously distributed throughout the meal being evaluated. Markers are available to measure emptying of specic meal components e solid, liquid or fat e but these must be
bound tightly to that component. Simultaneous measurement of
gastric emptying of solid and liquid meal components can be performed but requires the use of two radioisotopes. For single isotope
studies, the radioisotope selected should ideally have a half-life of
4e12 h, which allows adequate time for data acquisition without
excessive radiation. Our experience is that the time period for data
acquisition should be substantially longer than that used in health,
because the emptying rate is so slow in the critically ill, and
extended periods (of up to 6 h) are required to quantify any
emptying.
Radioisotopic data are then analysed using dedicated computer
software. Using a computer display, a region-of-interest is drawn
around the stomach, excluding the small intestine. This can be
difcult when there is overlying bowel and represents a potential
source of inaccuracy. Radioactive counts throughout the study are
then measured within the region-of-interest and corrected subsequently for isotope decay and tissue attenuation (i.e. depthrelated changes in activity), as both may substantially alter results [19]. In health, radioactivity may be corrected for tissue
attenuation using factors derived from a lateral image or using the
geometric mean of concurrent anteroposterior images [20]. In the
critically ill, lateral images are difcult or impossible to attain and
correction factors are frequently not performed. The left anterior
oblique (LAO) position is a simple method for correcting for
559
Fig. 1. a) Normal and delayed gastric emptying of 100 ml of liquid nutrient (2 kcal/ml) measured in two critically ill patients (unpublished data) over 5 h. On the rst image after the
meal is administered a region of interest (ROI) is drawn around the entire stomach contents. The images in 1a reveal a relatively normal rate of gastric emptying in a patient. The
radiolabelled meal progresses from the stomach into the small intestine across each image (with image acquisition taken at 1 h intervals). Figure. 1b) shows delayed gastric emptying
in the critically ill patient, with the radiolabelled being almost completed retained in the (proximal) stomach and radioisotope is only sparsely viewed distal to the pylorus.
560
Several groups, including ours, have used scintigraphy to measure gastric emptying in critically ill patients (Table 2) [3,5,23e26].
The precision associated with this technique allows it to determine
the effect of drugs that may have a small, but clinically important,
gastrokinetic effect. However, in most centres scintigraphy involves
transporting the patient to the nuclear medicine department,
limiting its use, however, mobile cameras, when available, obviate
the need to move a critically ill patient.
2.4. Indirect tests of gastric emptying
Indirect tests use a marker that is not absorbed in the stomach,
but is absorbed in the duodenum. Accordingly, the appearance of
the marker in blood, or a metabolite excreted by the lungs or kidneys, correlates with the rate of gastric emptying.
2.5. Drug absorption (paracetamol)
Fig. 2. a) Retention of gastric contents over time via scintigraphic technique. Data from
two critically ill patients after administration of 100 ml of liquid nutrient (2 kcal/ml)
labelled 20 MBq 99mTc- calcium phytate (unpublished data). A higher percentage of
contents retained in the stomach over time indicate a slower rate of gastric emptying
(solid circles). In a patient exhibiting normal gastric emptying (open circle) a lesser
percentage of the meal is retained over time. b) Cumulative dose of 13CO2 exhaled over
time. This gure displays data from the same two patients after administration of
100 ml of liquid nutrient (2 kcal/ml) labelled with 100 mcg of octanoic acid. The
octanoic acid contains 13C, which is absorbed by the small intestine and undergoes
hepatic metabolism to 13CO2, which is then exhaled. An increased amount of exhaled
13
CO2 indicates faster gastric emptying (open circles). Data from a patient with delayed
gastric emptying (solid circles) displays a lesser cumulative dose/hour of CO2 exhaled.
Due to the small change in cumulative dose from baseline in patients with very slow
gastric emptying, this measure may be less precise when measuring markedly delayed
gastric emptying.
Table 2
Scintigraphy as a measure of gastric emptying in the critically ill.
Study
Primary investigator (year)
Dose administered
(MBq)
Radionuclide used
Outcomes reported
Ott (1991)
18.5e37
99m
20e60 min
T50
20
18.5
20
20
20
99m
120 min
30 min
240 min
240 min
240 min
T50
T50
Ret
Ret
T50, Ret
Spapen (1995)
Kao (1998)
Nguyen (2008)a
Chapman (2009)a
Chapman (2011)a
a
Tc-diethylene-triamine-pentaacetic
acid (DTPA)
Tc-sulphur colloid
99m
Tc-phytate
99m
Tc-sulphur colloid
99m
Tc-sulphur colloid
99m
Tc-sulphur colloid
Denotes investigators from the same group; T50, scintigraphic half emptying time; Ret, intragastric content retention.
561
Table 3
Paracetamol absorption as a measure of gastric emptying in the critically ill.
Primary investigator
(year)
Dose administered
(mg)
Formulation of paracetamol
administered
S soluble
L liquid
Outcomes reported
Heyland (1996)
Tarling* (1997)
Goldhill* (1997)
McArthur (1995)
1600
1000
1000
1000
L
S
S
S
AUC120
AUC60
Cmax, Tmax and AUC60
Cmax, Tmax and AUC30 AUC180
Cohen (2000)
Jooste (1999)
MacLaren^ (2000)
MacLaren^ (2008)
Lucey (2003)
Marino (2003)
Tamion (2003)
1000
1500
1000
975
1500
1000
1000
L
S
L
L
L
S
S
AUC60
Cmax, AUC120
Tmax AUC120
Cmax, Tmax and C60 AUC60
AUC120
AUC120
Cmax, Tmax and AUC60 AUC180
A lack of standardisation is apparent between investigators using the paracetamol absorption test to measure gastric emptying in the critically ill. The dose of paracetamol
administered has ranged from 975 to 1600 mg, and some investigators administered the liquid suspension paracetamol, whereas others use dissolved tablets. There is also a
lack of consistency across studies in terms of the timing of measurements of plasma concentrations and outcomes reported.
*,^ Denotes investigators from the same group; Cmax, peak concentration of paracetamol; Tmax time to peak concentration; AUC area under curve.
Table 4
Breath test as a measure of gastric emptying in the critically ill.
Study
Primary investigator (year)
Dose administered
Outcomes reported
Ritz (2001)a
100 mL
13C-octanoic acid
GEC, t1/2
Chapman (2003)a
100 mL
13C-octanoic acid
Ritz (2005)a
100 mL
13C-octanoic acid
100 mL
13C-octanoic acid
Deane (2010)a
100 mL
13C-octanoic acid
Chapman (2011)a
75 KBq
14C-octanoic acid
Hr
Hr
Hr
Hr
Hr
Hr
Hr
Hr
Hr
Hr
Hr
Hr
Chapman (2005)
0e1:
1e4:
0e1:
1e4:
0e1:
1e4:
0e1:
1e4:
0e1:
1e4:
0e1:
1e4:
5 minutely
15 minutely
5 minutely
15 minutely
5 minutely
15 minutely
5 minutely
15 minutely
5 minutely
15 minutely Hr 4e5.5: 30 minutely
10 minutely
15 minutely
Denotes investigators from the same group; GEC, gastric emptying coefcient; t1/2 gastric half-emptying time.
GEC, t1/2
GEC, t1/2
GEC
GEC
GEC, t1/2
562
[4]
[5]
[6]
[7]
[8]
[9]
[10]
[11]
[12]
[13]
[14]
[15]
[16]
[17]
[18]
[19]
[20]
None.
Acknowledgment
PK is supported by a Royal Adelaide Hospital A.R. Clarkson
Scholarship. AMD is supported by a National Health and Medical
Research Council Early Career Fellowship.
[21]
[22]
[23]
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