WALTHAM International Science Symposium:
Nature, Nurture, and the Case for Nutrition
Gastric Emptying Rate Is Inversely Related to Body Weight in Dog Breeds of
Edwige Bailhache,* Mickae
Vincent Biourge,** Lucile Martin,*
National Veterinary School of Nantes, Laboratory of Nutrition and Endocrinology, Nantes, France,
Nutrition Research Centr e, Nan tes, France, and
Royal Canin Research Centre, Aimargues, France
When fed an identical diet, large and giant breeds of dog tend
to defecate more frequently and produce feces that have higher
water content and are of a poorer quality (softer) than smaller
breeds (1–4). However, the reason for the effect of body size on
fecal variables in otherwise healthy dogs remains unknown.
With such a huge range of body sizes (1–100 kg), different
breeds of dog might be expected to differ in many aspects of
gastrointestinal physiology. Larger breeds have a proportionately
smaller gastrointestinal tract, comprising 3–4% body weight
compared to 6–7% BW in smaller breeds (5). Previous
studies showed little effect of canine BW on orocecal transit time
(3,6), fecal microﬂora proﬁle (7), or small intestinal absorption
(4). However, a study using the lactulose to
excretion test found that small intestinal permeability was
greater in larger breeds of dog (4), and this may contribute, at
least in part, to the poor feces quality of larger dogs.
Gastric emptying rate (GER) is the speed with which
substances leave the stomach after ingestion. Liquids are re-
tained for the shortest period, followed by small then large solid
particles. GER is also affected by food-speciﬁc factors including
fat content. It could be hypothesized that size-related differ-
ences in GER might contribute to the poorer feces quality of
Nuclear scintigraphy was considered to be the ‘‘gold
standard’’ method for the measurement of GER, and was
validated in humans and dogs; when compared with other
methods in these species the technique provides the best
evaluation of GER (8,9). However, the cost of equipment and
use of radioactivity limit its use, and alternative methods was
therefore developed so as not to expose patients to high doses of
radiation. These methods include the use of the radio-opaque
markers and the
C-octanoic acid breath test (OABT). Both
have been compared to scintigraphy and validated in humans
and animals (10,11).
A previous study of gastric emptying time (GET), measured
by tracking the progress of radio-opaque markers from the
stomach into the small intestine, in four breeds of dog, aged
12–60 wk, found no effect of BW (3). However, the behavior of
such markers may not reﬂect that of food, because they cannot
be broken down by the mechanical action of the stomach. Large
markers are therefore retained for a disproportionately long time,
whereas small markers empty very quickly, probably during
liquid phase emptying. Intermediate-sized markers more accu-
rately reﬂect food, but the GET measured by this method shows
considerable intra- and inter-individual variation (11,12).
The OABT was used for measuring GER in many species
including humans, rat (13), cat (14), and dog (15). The test
involves monitoring the concentration of
in expired air
after ingestion of a meal labeled with
medium-chain fatty acid is rapidly absorbed from the
duodenum after gastric emptying of the test meal and carried
to the liver where it is quickly and completely oxidized to
carbon dioxide that is then exhaled in the breath. The rate of
in breath air would reﬂect the rate and
pattern of gastric emptying because gastric emptying would be
the limiting step in the digestion and metabolism of octanoic
acid (16). The method has advantages over the radio-opaque
Presented as part of the WALTHAM International Science Symposium:
Nature, Nurture, and the Case for Nutrition held in Bangkok, Thailand, October
28–31, 2003. This symposium and the publication of the symposium proceedings
were sponsored by the WALTHAM Centre for Pet Nutrition, a division of Mars,
Inc. Symposium proceedings were published as a supplement to The Journal of
Nutrition. Guest editors for this supplement were D’Ann Finley, James G. Morris,
and Quinton R. Rogers, University of California, Davis.
Financial support for this study was provided by Royal Canin, Aimargues,
J. Bourreau and D. Hern ot contributed equally to this work.
To whom correspondence should be addressed. E-mail: pnguyen@
Abbreviations used: APE, atom percent excess; BW, body weight; GER,
gastric emptying rate; GET, gastric emptying time; OABT, octanoic acid breath
0022-3166/04 $8.00 Ó 2004 American Society for Nutritional Sciences. J. Nutr. 134: 2039S–2041S, 2004.
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marker technique because the label is incorporated into
a standard meal. It is also noninvasive and uses a stable
isotope. A recent study using this test in dogs showed a weak
correlation between BW and GET (P 5 0.1) with an unusual
dog meal of bread, milk, and margarine (10).
The aim of this study was to measure the GET of a
conventional dog food, in 24 healthy adult dogs ranging in BW
from 3.5 to 59 kg, using the
C-octanoic acid breath test.
MATERIALS AND METHOD S
Twenty-four healthy adult dogs (2 males and 22 females, aged 4.0
6 0.3 y, BW 25.96 6 3.75 kg (range 3.5–59.1 kg) were recruited,
representing six breeds: Miniature Poodle (n ¼ 3), Beagle (n ¼ 1),
Schnauzer (n ¼ 6), Giant Schnauzer (n ¼ 5), Great Dane (n ¼ 5),
Labrador Retriever (n ¼ 3), Argentine Dane (n ¼ 1). Labrador
Retrievers and the Argentine Dane were loaned to the school by
private owners. Other dogs were owned by the National Veterinary
School of Nantes, where all dogs were housed for the duration of the
study. All experimental protocols were approved by the Animal Use
and Care Advisory Committee of the Nantes Veterinary School, and
adhered to European Union guidelines.
GET was assessed on a single occasion in each dog using a test meal
consisting of a commercially available extruded (dry) food (Maxi Adult
Young, Royal Canin, Aimargues, France; 25.7% crude protein, 15.2%
ether extract, 7.5% total dietary ﬁber, 1.71 MJ ME/100 g). After a 12-h
fast, each dog was given half its daily estimated energy requirement
(i.e., 276 kJ ME/kg BW
), labeled with sodium
(7.5 mgkg BW
; sodium octanoate 1-
C, 99% atom
Gif-sur-Yvette, France). To increase retention of the isotope in the
solid phase, the octanoate was added to egg yolk (2.64 g/kg BW
which was mixed with the test meal and then baked in a microwave,
before immediately feeding to the dog. All dogs had constant access to
water throughout the study, but were not allowed to eat anything other
than the test meal and were conﬁned to their kennel.
GET was assessed using the sodium
C-octanoate breath test.
Dogs were maintained in a quiet environment, to maintain a constant
carbon dioxide production rate. After appropriate habituation training
of the dogs to the apparatus, duplicate samples were obtained at
; immediately before ingestion of the test meal). Duplicate
samples were then taken for the 6-h period after ingestion of the test
meal: every 15 min for 4 h, and every 30 min for the ﬁnal 2 h of the
Breath samples were collected using an anesthetic mask (Canine
Ventilation/Anesthesia Mask, Harvard Apparatus, Les Ulis, France)
connected to a 2-L Douglas rubber bag (Fisher Scientiﬁc Labosi,
Elancourt, France) by a two-way valve (Two-Way Non-Rebreathing
Valve, Harvard Apparatus, Les Ulis, France). This system allowed the
dogs to breathe normally, while expired air only was collected in the
bag. The mask was ﬁtted snuggly around the muzzle, and the dog was
allowed to breathe normally until the reservoir bag was ﬁlled.
Duplicate samples of the expired air were withdrawn from the bag
using 20-mL syringes and a three-way tap. The syringes were sealed
using a second three-way tap, and the samples were immediately
transferred to sealed vials (HexatainerÒ, Labco, Buckinghamshire,
UK); these were stored at room temperature for up to 4 wk before
The ratio of
in the breath samples (ppm) was
determined by gas chromatography-isotope ratio-mass spectrometry
(BreathmatÒ, Finnigan, Bremen, Germany) and then converted to
APE (atom percent excess). The net effect of the test meal was ob-
tained by subtracting the baseline (T
) values for each dog.
excretion curve (APE against time) was ﬁtted as
described previously (15), and the area under the curve used to
determine gastric emptying characteristics. The time at which 25%
), 50% (T
), and 75% (T
) of the area under the curve was
reached and the time corresponding to peak excretion (T
calculated. These coefﬁcients were each plotted against BW and
assessed by regression to determine if any relationship was present.
The data are presented as mean
SEM, and P , 0.05 was considered
Overall, excretion of 25% of the octanoate dose (T
85 6 4 min. Fifty percent of the dose was excreted in 154 6 5
) and 75% of the dose in 240 6 6 min (T
excretion occurred at 91 6 9 min (T
was signiﬁcantly longer in the larger dogs. Hence, there
was a signiﬁcant positive linear correlation between BW and
(r ¼ 0.76, P , 0.0001) (Fig. 1), and between BW and
(r ¼ 0.67, P ¼ 0.0004).
was also signiﬁcantly longer in larger dogs. Hence,
there was a signiﬁcant positive linear correlation between BW
(r ¼ 0.46, P ¼ 0.02), and a signiﬁcant positive
polynomial correlation (GET ¼ 78.80 1.38*BW 1
) between BW and T
(r ¼ 0.78, P , 0.0001)
We used the OABT to compare the gastric emptying pattern
in dogs differing in body size. It has been shown that postgastric
C-octanoic acid and subsequent
exhalation occurs very rapidly, and with minimal inter-subject
variability (17). Octanoic acid is rapidly absorbed from the
intestine and carried via the portal vein to the liver where it
rapidly undergoes b-oxidation. A peak excretion of
been observed ;12 min after intraduodenal administration of
C-octanoic acid in human volunteers (16). In a dog
appeared 15 min earlier in saliva than
in breath air after
oral administration of [
C] octanoic acid, due to in-
into the bicarbonate pool (18). Gastric
emptying measured using OABT is then delayed compared to
scintigraphy. A 69-min difference in the half-emptying times
between these two methods was reported (19). It was neverthe-
less shown that the gastric emptying pattern was similar when
determined simultaneously by both these methods (16).
Large dogs had a longer GET at every sample point, compared
to small dogs, when fed a commercial extruded dog food. This
means that in large breeds of dog, food is retained in the stomach
for a longer period; they have a lower rate of gastric emptying.
These ﬁndings are in contrast with those of a previous study in
dogs that failed to ﬁnd any correlation between BW and GET
(3). However, a strong inverse relationship was identiﬁed in
a study in humans weighing 59–93 kg (20). A weak correlation
was reported in dogs weighing 13.5–37 kg (21), and also in
another dog study (n ¼ 60), although the weight range was not
Compared with a previous study using the OABT (15), GET
in the current study was much shorter. This could be explained
FIGURE 1 Time at which 25% (T
) of the area under the curve of
was reached after ingestion of a single meal labeled with
C-octanoic acid in dogs of varying body weight.
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by differences between the test meals used; although the energy
allowance was similar, the composition was different. Thus, the
test meal used in the Wyse et al. study consisted of whole-meal
bread, skimmed milk, and sunﬂower margarine (15), compared
to a conventional dog food in this study. The bread, milk, and
margarine test meal would contain more fat, which is known to
slow gastric emptying and could lead to longer emptying time.
All of these factors could explain the differences between the
previous results and ours.
The stomach is a muscular bag with several roles in digestion.
It stores food temporarily and participates in the initial stages of
digestion including denaturation and predigestion of proteins.
Contractions of the muscular walls facilitate the mixing and
maceration of ingesta then the formation of the chyme. The
stomach also controls the rate of entry of the chyme into the
small intestine. Relatively premature gastric emptying may
discharge inadequately predigested particles. A high emptying
rate may overload the small intestine. Either of these cir-
cumstances would be likely to occur in small breed dogs.
Premature discharged and/or overloading particles would be less
susceptible to intestinal enzymatic hydrolysis, and so they may
pass relatively undigested into the large bowel. The microﬂora
residing there utilize nitrogen and carbohydrate sources to
produce metabolites, which can affect colonic absorption and
physiology, a major determinant of feces quality (22). It would
therefore be possible that gastric emptying time might alter the
physiology of the large intestine. Some digestive troubles would
then be expected in small dogs, in which GER was higher. The
fact is that small breed dogs did not generally experience any
fecal consistency problem, whereas large dogs did. Our results
concerning the GET of different breeds therefore fail to explain
the higher water content and lower stool quality in large dogs.
The factors causing poor feces quality in otherwise healthy,
large breed dogs are therefore unknown, although increased
small intestinal permeability in large breeds has been correlated
with fecal moisture content (4). No such relationship has been
demonstrated between GER and fecal variables in normal
subjects, although ileojejunal transposition both delays gastric
emptying of solids and decreases fecal water content in dogs
with total colectomy (23). Puppies are well known for their
poor feces quality (3), and also have higher GER than adults
(3), but the two are not correlated. This supports previous work
in humans, where feces quality was not related to GER (24).
Further work is required to establish if there is a direct
(causative) link between GER and fecal variables.
In summary, the GET in large breed dogs was longer than
that in smaller dogs, and this would not be likely to contribute
to the poor feces quality associated with higher body weight.
The authors are grateful to Samuel Ninet and Ge
rald Pondevie for
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FIGURE 2 Time at which peak excretion of
) after ingestion of a single meal labeled with
C-octanoic acid in
dogs of varying body weight.
2041SGASTRIC EMPTYING RATE AND BODY WEIGHT IN DOGS
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