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Gastric Emptying Rate Is Inversely Related to Body Weight in Dog Breeds of Different Sizes

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WALTHAM International Science Symposium:
Nature, Nurture, and the Case for Nutrition
Gastric Emptying Rate Is Inversely Related to Body Weight in Dog Breeds of
Different Sizes
1,2
Jarno Bourreau,*
3
David Hernot,*
3
Edwige Bailhache,* Mickae
¨
l Weber,*
Ve
´
ronique Ferchaud,
y
Vincent Biourge,** Lucile Martin,*
y
Henri Dumon,*
y
and
Patrick Nguyen*
y4
*
National Veterinary School of Nantes, Laboratory of Nutrition and Endocrinology, Nantes, France,
y
Human
Nutrition Research Centr e, Nan tes, France, and
**
Royal Canin Research Centre, Aimargues, France
EXPANDED ABSTRACT
KEY WORDS:
gastric emptying
body weight
dog
feces
Introduction
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
(BW)
5
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
L-rhamnose urinary
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
larger dogs.
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
13
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
13
CO
2
in expired air
after ingestion of a meal labeled with
13
C-octanoate. This
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
appearance of
13
CO
2
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
1
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.
2
Financial support for this study was provided by Royal Canin, Aimargues,
France.
3
J. Bourreau and D. Hern ot contributed equally to this work.
4
To whom correspondence should be addressed. E-mail: pnguyen@
vet-nantes.fr.
5
Abbreviations used: APE, atom percent excess; BW, body weight; GER,
gastric emptying rate; GET, gastric emptying time; OABT, octanoic acid breath
test.
0022-3166/04 $8.00 Ó 2004 American Society for Nutritional Sciences. J. Nutr. 134: 2039S–2041S, 2004.
2039S
by guest on April 11, 2016jn.nutrition.orgDownloaded from
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
13
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
0.75
), labeled with sodium
13
C-octanoate
(7.5 mgkg BW
0.75
; sodium octanoate 1-
13
C, 99% atom
13
C, Euriso-top,
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
0.75
),
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
13
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
baseline (T
0
; 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
test.
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
analysis.
The ratio of
13
CO
2
:
12
CO
2
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
0
) values for each dog.
The
13
CO
2
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%
(T
0.25
), 50% (T
0.50
), and 75% (T
0.75
) of the area under the curve was
reached and the time corresponding to peak excretion (T
max
) were
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
significant.
RESULTS
Overall, excretion of 25% of the octanoate dose (T
0.25
) took
85 6 4 min. Fifty percent of the dose was excreted in 154 6 5
min (T
0.50
) and 75% of the dose in 240 6 6 min (T
0.75
). Peak
excretion occurred at 91 6 9 min (T
max
).
T
0.25
was significantly longer in the larger dogs. Hence, there
was a significant positive linear correlation between BW and
T
0.25
(r ¼ 0.76, P , 0.0001) (Fig. 1), and between BW and
T
0.50
(r ¼ 0.67, P ¼ 0.0004).
T
0.75
was also significantly longer in larger dogs. Hence,
there was a significant positive linear correlation between BW
and T
0.75
(r ¼ 0.46, P ¼ 0.02), and a significant positive
polynomial correlation (GET ¼ 78.80 1.38*BW 1
0.05*BW
2
) between BW and T
max
(r ¼ 0.78, P , 0.0001)
(Fig. 2).
DISCUSSION
We used the OABT to compare the gastric emptying pattern
in dogs differing in body size. It has been shown that postgastric
processing of
13
C-octanoic acid and subsequent
13
CO
2
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
14
CO
2
has
been observed ;12 min after intraduodenal administration of
14
C-octanoic acid in human volunteers (16). In a dog
2
H
2
O
appeared 15 min earlier in saliva than
13
CO
2
in breath air after
oral administration of [
2
H/
13
C] octanoic acid, due to in-
corporation of
13
CO
2
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
indicated (10).
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
0.25
) of the area under the curve of
breath
13
CO
2
was reached after ingestion of a single meal labeled with
13
C-octanoic acid in dogs of varying body weight.
2040S SUPPLEMENT
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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.
ACKNOWLEDGMENT
The authors are grateful to Samuel Ninet and Ge
´
rald Pondevie for
technical assistance.
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FIGURE 2 Time at which peak excretion of
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CO
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was reached
(T
max
) after ingestion of a single meal labeled with
13
C-octanoic acid in
dogs of varying body weight.
2041SGASTRIC EMPTYING RATE AND BODY WEIGHT IN DOGS
by guest on April 11, 2016jn.nutrition.orgDownloaded from
... The rate of gastric emptying (GE) and the concentrations of postprandial glucose (PPG), which are directly associated in humans, may contribute to the onset of obesity and its secondary complications in canines [5,6]. Gastric emptying rate (GER) is defined as the speed with which nutrients are released from the stomach into the duodenum of the small intestine following ingestion [7]. A faster GER results in higher PPG concentrations [5]. ...
... In order to assess the rate of GE, several approaches have been investigated. Gamma Scintigraphy (GS) is considered by many to be the "gold standard" method to measure GE; however, this approach is fairly expensive and involves radiation exposure [7]. Acetaminophen (Ac) tracking is a method based on the understanding that Ac is slowly absorbed from the stomach but rapidly absorbed in the small intestine [21]. ...
... Acetaminophen (Ac) tracking is a method based on the understanding that Ac is slowly absorbed from the stomach but rapidly absorbed in the small intestine [21]. This approach is significantly less expensive than GS and involves no radiation exposure [7]. Additionally, a study completed by Glerup et al. in 2007 compared three different methods used to assess GE in research animals, including GS, Ac tracking, and the 13 C-acetate breath test, and found that the results obtained from Ac tracking were similar to the results obtained via GS [22]. ...
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... The rate of gastric emptying (GE) and the concentrations of post-prandial glucose (PPG), which are directly associated in humans, may contribute to the onset of obesity and its secondary complications in canines [5,6]. Gastric emptying rate (GER) is defined as the speed with which nutrients are released from the stomach into the duodenum of the small intestine following ingestion [7]. A faster GER results in higher PPG concentrations [5]. ...
... In order to assess the rate of GE, several approaches have been investigated. Gamma Scintigraphy (GS) is considered by many to be the "gold standard" method to measure GE; however, this approach is fairly expensive and involves radiation exposure [7]. Acetaminophen (Ac) tracking is a method based on the understanding that Ac is slowly absorbed from the stomach but rapidly absorbed in the small intestine [20]. ...
... Acetaminophen (Ac) tracking is a method based on the understanding that Ac is slowly absorbed from the stomach but rapidly absorbed in the small intestine [20]. This approach is significantly less expensive than GS and involves no radiation exposure [7]. Additionally, a study completed by Glerup et al. in 2007 compared three different methods used to assess GE in research animals, including GS, Ac tracking and the 13 C-acetate breath test, and found that the results obtained from Ac tracking were similar to the results obtained via GS [21]. ...
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... Bourreau et al. (38) has previously explained that a high gastric emptying rate might overload the small intestine of smaller canines due to discharge of inadequately pre-digested food particles. These food particles are generally less susceptible to intestinal enzymatic hydrolysis and remain undigested. ...
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... Miniature Poodle, Standard Schnauzer, Giant Schnauzer and Great Danes) using radiopaque markers ingested with food (T50 = 6.4-7.8 h). Without specifying any values, Bourreau et al. [89] concluded on a longer GET in large compared to small breeds after ingestion of a dry food meal using breath test method. Contrarily, Boillat et al. [4] described a shorter GET in large compared to medium breeds (range 6.8-15 h), using wireless motility capsule immediately administered after a dry food meal. ...
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Health and well-being of dogs are of paramount importance to their owners. Digestion plays a key role in dog health, involving physicochemical, mechanical and microbial actors. However, decades of breeding selection led to various dog sizes associated with different digestive physiology and disease sensitivity. Developing new products requires the consideration of all the multi-faceted aspects of canine digestion, the evaluation of food digestibility, drug release and absorption in the gut. This review paper provides an exhaustive literature survey on canine digestive physiology, focusing on size effect on anatomy and digestive parameters, with graphical representation of data classified as "small", "medium" and "large" dogs. Despite the huge variability between protocols and animals, interesting size effects on gastrointestinal physiology were highlighted, mainly related to the colonic compartment. Colonic measurements, transit time permeability, fibre degradation, faecal short-chain fatty acid concentration and faecal water content increase while faecal bile acid concentration decreases with body size. A negative correlation between body weight and Proteobacteria relative abundance was observed suggesting an effect of dog body size on faecal microbiota. This paper gathers helpful in vivo data for academics and industrials and supports the development of new food and pharma products to move towards canine personalized nutrition and health.
... Most available in vitro models, and especially the more complex FIDO and M-SCIME systems, have been designed to reproduce a medium-sized dog's digestive conditions when ingesting dry food. As widely described, canine digestion is impacted by body weight or breed (Kendall et al., 1983;Bourreau et al., 2004;Hernot et al., 2005;Weber, 2006;Weber et al., 2017). Considering the influence of body weight and/or breed on canine digestive physicochemical and microbial parameters is undoubtedly a promising line of research to develop more relevant in vitro models. ...
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Dogs occupy a full place in the family and their well-being is of paramount importance to their owners. Digestion, a complex process involving physicochemical, mechanical, and microbial parameters, plays a central in maintaining animals healthy. As in vivo studies in dogs are more and more restricted by ethical, regulatory, societal, and cost reasons, an alternative option resides in the use of in vitro models simulating the different parts of the canine gastrointestinal tract. This review paper first introduces digestion and gut microbiota as key factors in dog nutrition and health, under both healthy and diseased conditions (obesity and inflammatory bowel disease), by highlighting when relevant similarities or differences between human and canine digestion process. Then, we provide for the first time an in-depth description of currently available models of the canine digestive tract, discuss technical and scientific challenges that need to be addressed and introduce potential applications of in vitro gut models in food and veterinary fields. Even if the development of some in vitro models remains limited by a lack of in vivo data in dogs necessary for a relevant configuration and validation, translation of long-term expertise on human in vitro gut models to dog's ecosystem opens avenues for canine in vitro gut model development and their adaptation to specific digestive conditions associated to various ages, sizes, breeds and/or diets, under both physiological and diseased states.
... These evaluations may not be suitable for ensuring the same safety, absorption, and bioavailability characteristics in different species (Toutain and Koritz,1997;Fleischer et al., 2008;Apley et al., 2017). These problems, which are related to the different physiology and the different transit time of the gastrointestinal tract (Dressman, 1986;Bourreau et al., 2004;Apley et al., 2013;Weber et al., 2017) become particularly critical for smaller animals, precisely those that need the most precise adjustment of the dose by splitting the tablets even in several pieces. The price of the pharmaceutical product is generally more linked to the production of the dosage unit rather than the content of active molecule: for many drugs, 10 tablets containing 10 mg of active have a price comparable to 10 units containing 20 mg of active (Bachynsky et al., 2002). ...
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... familiaris) associated with different breeds. The effect of canine body size on gastrointestinal transit has been adressed but results are contradictory, with some authors finding an inverse relationship of gastric emptying and body size (Bourreau et al., 2004) whereas others could not find any relation (Weber et al., 2002b;Yam et al., 2004;. ...
... Data on the weight of digestive tract are rather scarce indeed and, in most cases, one has to recalculate relative weights from available absolute values. In leporids stomach and intestine comprise together from 10 to 20% of the body weight (Meredith, 2010;Jin et al., 2014), while in felidae and domestic dogs this value is normally below 6% (Crile and Quiring, 1940;Chivers and Hladik, 1980;Bourreau et al., 2004). ...
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